The evolution and functional significance of the cetacean pelvic bones

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THE EVOLUTION AND FUNCTIONAL SIGNIFICANCE OF THE CETACEAN PELVIC BONES

by

James P. Dines

A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(INTEGRATIVE AND EVOLUTIONARY BIOLOGY)

August 2014

Copyright 2014 James P. Dines
i

Table of Contents
Epigraph ii
Dedication iii
Acknowledgments iv
List of Figures vi
List of Tables viii
Abstract ix
Chapter One: Introduction 1
Chapter Two: The Progressive Reduction of the Cetacean Pelvic Girdle 9
Chapter Three: Analysis of Cetacean Pelvic Bones: Challenges and Solutions 40
Chapter Four: Testes Evolution and Mating Strategies in Cetaceans 67
Chapter Five: Cetacean Pelvic Bones Respond to Sexual Selection 103
Chapter Six: Conclusions 181
Combined Bibliography 188
Appendix: Specimens Examined 220

ii

Epigraph

Nothing can be imagined more useless to the animal than rudiments of hind legs entirely buried
beneath the skin of a whale, so that one is inclined to suspect that these structures must admit
of some other interpretation.

Prof. John Struthers, 1881, On the Bones, Articulations,
and Muscles of the Rudimentary Hind-Limb of the
Greenland Right Whale (Balaena mysticetus).
iii

Dedication

To my family.

iv

Acknowledgements
I am grateful for the guidance, encouragement, and insights of my dissertation committee:
Cheng-Ming Chuong, Matt Dean, Jill McNitt-Gray and Xiaoming Wang. A very special thank you
is extended to Matt Dean for welcoming me into his lab discussion groups, for his boundless
and quite contagious enthusiasm, for his friendship, and for showing me that “doing cool
science” is really what it’s all about.
For access to collections, loans of specimens, and overall generosity, I am indebted to my
museum colleagues: Charley Potter and John Ososky (Smithsonian Institution), Richard Sabin
(British Museum), Tom French (Massachusetts Department of Fish and Wildlife), Kate Doyle
(University of Massachusetts-Amherst), Jeff Bradley (University of Washington Burke Museum
of Natural History), Moe Flannery (California Academy of Sciences), Thor Holmes (Humboldt
State University Vertebrate Museum), and Sue McLaren (Carnegie Museum of Natural History).
Erik Otárolo-Castillo (Harvard University) provided generous assistance in helping me to
understand and perform geometric morphometric analyses, and allowed me to test early
versions of his landmark digitization program.
Thanks are extended to Dave Janiger for preparation of specimens and diligently “saving the
pelvic bones” for me, for his invaluable digital reference archive, for sharing his knowledge of
cetacean anatomy, and for his cheerful spirit and friendship. Thanks are also extended to
Kimball Garrett for encouragement and friendship over the years.
Thank you to Ed Mitchell for many valuable discussions on cetacean evolution and anatomy, for
evaluating various manuscript versions, for his entertaining stories, for general mentorship, and
v

for being a good friend. Ed Mitchell and Mike Bell provided early inspiration for the study of
pelvic bones in dolphins.
Tim Daley, Andrew Smith, and Peter Ralph provided invaluable computational and theoretical
assistance. Francisco Rojas assisted in 3D laser scanning. Jesse Alas assisted in data entry.
Members of the Dean Lab and the Molecular and Computational Biology discussion group are
thanked for providing useful dialog, camaraderie, and support.
Neil Ives and Gary Stupien from Aerospace Corporation are thanked for generously providing
time on their high resolution CT scanners. Giarr-Ann Kung from the Natural History Museum of
Los Angeles County is thanked for arranging and assisting in the CT scanning sessions.
For financial support, I thank the USC Integrative and Evolutionary Biology Program, the USC
Ecology and Biodiversity Initiative, and the William Cheney, Jr. Memorial Fund for Mammalogy.
Matt Dean, Ed Mitchell and Michelle Dines provided generous and valuable editorial guidance.
Lastly, I am fortunate to have a loving and supportive family, all of whom inspired me
throughout this incredible journey. Thank you all.

vi

List of Figures
Figure 2.1 Variation in odontocete pelvic bones ................................................................... 35
Figure 2.2 Remnant hind limb structures in modern cetaceans ................................................ 36
Figure 2.3 Penis of a gray whale, Eschrichtius robustus, attached to the two pelvic bones. . 37
Figure 2.4 Penis and associated structures of a fin whale, Balaenoptera physalus .............. 38
Figure 2.5 Penis and associated structures of a long-beaked common dolphin,
Delphinus capensis ............................................................................................... 39
Figure 3.1 Digital models of a pelvic bone from a Dall’s porpoise (LACM 54420,
Phocoenoides dalli)………………………………………………………………………………………….. 58
Figure 3.2 Three-dimensional mesh model of the right pelvic bone from a long-beaked
common dolphin (LACM 96366, Delphinus capensis) ............................................... 59
Figure 3.3 Three-dimensional mesh model of the right first vertebral rib from a long-
beaked common dolphin (LACM 96366, Delphinus capensis) ................................. 60
Figure 3.4 Transforming and defining landmarks on pelvic bones ....................................... 61
Figure 3.5 Transforming and defining landmarks on ribs ..................................................... 63
Figure 4.1 Relative testes mass among 133 mammalian species ......................................... 91
Figure 4.2 Relative sperm competition among 49 species in Cetacea ................................. 92
Figure 4.3 Tradeoff between investment in weapons and investment in testes ................. 95
Figure 5.1 Limb buds in a series of developing embryos of the pantropical spotted
dolphin, Stenella attenuata ....................................................................................... 149
vii

Figure 5.2 The relationship, after controlling for phylogeny, between relative testes
size and percentage of litters with multiple paternity in rodents ..................... 150
Figure 5.3 Cetacean phylogeny ........................................................................................... 151
Figure 5.4 The correlation of residual testis mass and residual penis length in
baleen whales ............................................................................................................. 152
Figure 5.5 Correlation of maximum testes mass and maximum body length .................... 154
Figure 5.6 Correlation of pelvic bone centroid size and maximum body length ................ 156
Figure 5.7 Correlation of pelvic bone centroid size residuals and testes mass residuals .. 158
Figure 5.8 Size and shape evolution of pelvic bones and ribs in relation to testes mass .. 159
Figure 5.9 Marginal posterior distribution of correlation coefficients, all adult males ..... 161
Figure 5.10 Marginal posterior distribution of correlation coefficients, adult males with
complete bones .................................................................................................. 162
Figure 5.11 The marginal posterior distribution of correlation coefficients, adult females 163

viii

List of Tables
Table 3.1 Specimens examined ………………………………………………………………………………………65
Table 3.2 Optimal scan parameters……………………………………………………………………….……..…66
Table 4.1 Mating systems…………………………………………….…………………………………………...…….97
Table 4.2 Body mass, testes mass, and testes residuals………….……………………………………….98
Table 4.3 Results from regression analyses………………………….………………………………………..102
Table 5.1 Morphological parameters of cetacean species……….……………………………….…….164
Table 5.2 List of specimens examined……………….…………………………………………………………..166
Table 5.3 Posterior means and quantiles, all adult male specimens…………………………..…..171
Table 5.4 Marginal posterior distributions of correlations, all adult male specimens…....172
Table 5.5 Posterior means and quantiles, adult male specimens with all bones………….…173
Table 5.6 Marginal posterior distributions of correlations, adult male specimens
with all bones……………………..………………………………………………………………………….174
Table 5.7 Posterior means and quantiles, adult female specimens..……………………………...175
Table 5.8 Marginal posterior distributions of correlations, adult female specimens….…..176
Table 5.9 ANOVA of pairwise differences in pelvic bone centroid size…………………….….….177
Table 5.10 ANOVA of pairwise differences in rib centroid size……………………………….….…….178
Table 5.11 ANOVA of pairwise differences in pelvic bone shape…………………………….….…….179
Table 5.12 ANOVA of pairwise differences in rib shape……………………………………………….…..180

ix

Abstract
Modern whales and dolphins evolved from four-legged terrestrial mammals known from
fossils that are 54 million years old. The gradual transition from living entirely on land to a fully
aquatic existence in cetaceans was accompanied by a mosaic of adaptations for efficient
locomotion in the marine environment. Among those adaptations are the progressive loss of
external hindlimbs and the reduction of the pelvic girdle to a pair of unconnected pelvic bones.
The remnant pelvic bones in cetaceans are often cited as useless vestigial structures, having no
function but providing a glimpse of their evolutionary history. However, the pelvic bones in
cetaceans, as in other tetrapods, are anchors for the genitalia and associated muscles. Cetacean
pelvic bones also exhibit remarkable variation in shape and size among species, a pattern
predicted by sexual selection theory. Sexual selection has been shown to influence the variation
in the morphology of genitals and other structures related to mating in groups spanning
invertebrates and vertebrates. The hypothesis that cetacean pelvic bones evolve in response to
sexual selection is tested herein.
The evolutionary history of cetaceans was reviewed, with special emphasis on tracing
the progressive loss of the hind limb elements and reduction of the pelvic girdle. Using museum
collections, more than 250 specimens representing 38 species were examined. Dissections on
dead-stranded cetacean carcasses provided new insights into pelvic bone orientation and
muscle attachments within the organisms. Among the challenges in performing a quantitative
analysis was the lack of identifiable landmarks in cetacean pelvic bones, which was resolved
using three-dimensional imaging technology and novel methods in geometric morphometrics.
x

Since mating ecology is essentially unknown in most cetacean species, the variation in the
relative size of testes among cetaceans was investigated. Relative testes size is a common proxy
of mating system across diverse taxa with internal fertilization and is validated for cetaceans
herein. For example, sperm competition theory predicts that species with promiscuous mating
systems will have large relative testes. Similarly, there is expected to be a trade-off between
investment in weapons used in pre-copulatory dominance contests and investment in testes
mass. Both patterns hold true for cetaceans. As predicted, the patterns of variation in cetacean
pelvic bones are correlated with variation in mating ecology, as inferred from relative testes
mass.
Cetaceans comprise a charismatic group of mammals that are an exemplar of natural
selection. A rich fossil record documents their transition from quadrupedal land-dwelling
species to the fully aquatic modern forms with streamlined bodies. Among the dramatic
morphologic changes in the evolutionary history of whales was the progressive loss of
hindlimbs and reduction in the pelvic girdle, a trend that culminated in a pair of greatly reduced
pelvic bones in modern species. Contrary to textbook descriptions, pelvic bones in modern
cetaceans are not useless vestiges. Rather, cetacean pelvic bones play an essential role in
mating ecology and reproductive fitness. In addition to pointing out the need to re-write
textbooks on evolution, this study is the first demonstration of sexual selection influencing
internal reproductive structures.

1

Chapter 1: Introduction
Modern whales and dolphins have a greatly reduced pelvic girdle, typically manifested
as a pair of rod-like “pelvic bones” that are dissociated from the vertebral column. Cetacean
pelvic bones are commonly cited as vestigial structures that provide a glimpse of the
evolutionary history of whales. An exceptional fossil record documenting the progressive
transition of cetaceans from land-dwelling quadrupeds to streamlined fully aquatic modern
forms lacking external hind limbs makes cetaceans a textbook example of organic evolution
(Ridley 2004). However, labelling cetacean pelvic bones as vestigial, or even as “useless
vestiges” (Curtis and Barnes 1989), implies that they are on an evolutionary trajectory of being
entirely lost.
However, cetacean pelvic bones have an important function: providing an anchor for
structures used in reproduction. As in other tetrapods, the bones of the cetacean pelvis are the
origins for the genitals and associated muscles. Cetacean pelvic bones may have lost their
function in locomotion, but they nevertheless retain their role in mating, making them uniquely
suited to test the influence of sexual selection on internal reproductive structures.
The thesis presented in this dissertation will demonstrate that cetacean pelvic bones not
only play a significant role in reproduction, they also exhibit remarkable morphologic
interspecific variation in response to sexual selection.
Cetacean evolutionary history is reviewed in Chapter Two. Distinctive reference is given
to changes in the structure of cetacean pelvic bones as they transitioned from an entirely
terrestrial mode of life to a fully aquatic lifestyle. The earliest whales appeared approximately
2

54 million years ago (Uhen 2010). From that point forward, a progressive reduction in the size
of the pelvic girdle occurred concomitantly with increased streamlining. Two major trends
were a great decrease in the size of hind limbs occurring between 48-42 million years ago, and
the entire loss of external hind limb elements, being wholly incorporated internally in an
unknown ancestor of modern cetaceans approximately 41 million years ago (Gatesy et al.
2013).
In addition to summarizing the evolutionary history of hind limb reduction in cetaceans,
Chapter Two describes the remarkable variation in the shape and relative size of pelvic bones
within and among modern cetacean species. Size and shape vary ontogenetically, with dramatic
increase in size and degree of ossification occurring at the onset of sexual maturity (Andersen
et al. 1992). Cetacean pelvic bones also exhibit sexual variation (Perrin 1975). The variation in
relative size and shape of pelvic bones between species is the most striking (see figure 2.1), a
pattern never before examined. Finally, Chapter Two provides anatomical evidence from fresh
dissections and from the literature that pelvic bones anchor the genitalia, suggesting an
important role in mating.
Chapter Three describes the challenges of analyzing cetacean pelvic bones. Pelvic bones
are rare in systematic collections, but more than 250 paired pelvic bone specimens from 38
species of cetaceans were obtained from museum collections. This included 9 mysticete (baleen
whale) species and 29 odontocete (toothed whale) species, comprising more than 40 percent of
the currently recognized modern species (Perrin 2014). Another challenge is that cetacean
pelvic bones lack homologous landmarks, features necessary for traditional morphometric
3

analyses. To resolve this dilemma, left and right pelvic bones from each cetacean specimen
were scanned using a NextEngine three-dimensional laser scanner (NextEngine Inc., Santa
Monica, CA). The use of surface data generated by 3D imaging provides a richer description of
overall shape than has been previously available for morphometric analyses and reduces the
need for homologous landmarks (Adams et al. 2004). Novel methods based on established
geometric morphometric approaches were collaboratively developed to analyze the acquired
surface scan data.
The surface scan data was transformed into landmarks and semi-landmarks, which were
used to statistically quantify the size and shape of the pelvic bones. Size was measured as
“centroid size” while shape differences were analyzed using Generalized Procrustes Analysis
(Slice 2007), a technique that computationally removes all “non-shape” variables from an
object prior to statistical analysis. In addition to the pelvic bones, the pair of first vertebral
ribs—when available from the same specimens—were subjected to the same analyses. Unlike
pelvic bones, ribs are not involved in reproduction and therefore are a useful control in the
analyses.
Relating cetacean pelvic bone morphology to sexual selection requires knowing
something about the mating ecology of whales and dolphins. Unfortunately, very little is known
about the mating systems of most species of cetaceans (Mesnick and Ralls 2009). Insights from
testes evolution, however, provide a way to predict mating strategies for taxa from which
information is unavailable. A large body of literature demonstrates a strong correlation
between relative size of testes and mating ecology. As sperm competition increases, there is
4

also an increase in relative testes mass (Parker 1984; Heske and Ostfeld 1990; Harcourt et al.
1995; Birkhead and Møller 1998; Hosken 1998; Hosken and Ward 2001; Byrne et al. 2002;
Ramm et al. 2005). In promiscuous mating systems with intense sperm competition males
exhibit large testes relative to body mass. Conversely, in mating systems with very little sperm
competition (e.g., monogamy), males have small relative testes.
Against this background, Chapter Four testes evolution in cetaceans is examined to
establish relative testes mass as a proxy for mating ecology. Data on testes mass and body mass
was collected from the literature for 49 species of cetaceans and examined with respect to
predictions from sperm competition theory. A regression of log body mass against log testes
mass was performed to predict the relationship between body mass and testes mass. Species
with testes mass larger than expected for their body (expressed as a positive residual value) are
expected to experience intense sperm competition (i.e., a promiscuous mating system).
Conversely, species with testes mass smaller than expected for their body (expressed as a
negative residual value) are expected to experience little or no sperm competition.
Also demonstrated from the analysis of testes mass is the trade-off between pre-
copulatory and post-copulatory traits, a pattern predicted by sperm competition theory
(Simmons and Emlen 2006). Cetaceans with tusks or battle teeth, used as weapons in
establishing dominance, have relative testes much smaller than expected for their body size.
Similarly, species in which males are larger than females or have other dimorphic features also
have testes smaller than expected for their body size. Large size is advantageous in dominance
5

battles among rival conspecific males; sexually dimorphic features like anal humps are potential
cues of an individual’s fitness to females or other males (Connor et al. 2000).
Information about mating ecology, as inferred from residual testes size, can be used to
explain variation in other structures used for reproduction. The hypothesis that size and shape
of cetacean pelvic bones is correlated with mating ecology was examined in Chapter Five. First,
in a re-analysis of data from Brownell and Ralls (1986), it was shown there is a positive
correlation between relative penis length and relative testes mass in cetaceans. That is, relative
penis length increases with increased promiscuity. It follows that the internal structure
supporting the penis—the pelvic bone—should also vary with degree of promiscuity. Using
geometric morphometric methods described in Chapter Two, the size and shape of cetacean
pelvic bones were analyzed in a phylogenetic context to test the relationship between mating
ecology and pelvic bone morphology.
Species inferred to operate in a promiscuous mating system, based on large relative
testes mass, exhibited large pelvic bones relative to their body size. In contrast, species with
small relative testes also had small pelvic bones relative to body size. Included in the latter
category are species like the franciscana dolphin, a species considered to be serially
monogamous (Panebianco et al. 2012), and most of the beaked whales, the males of which
apparently engage in pre-copulatory aggression to establish dominance . These patterns
demonstrate that cetacean pelvic bones are not useless vestiges, but instead play an important
role in mating ecology and have evolved in response to sexual selection.

6

Literature Cited

Adams, D. C., F. J. Rohlf, and D. E. Slice. 2004. Geometric morphometrics: ten years of progress
following the ‘revolution’. Italian Journal of Zoology 71:5-16.
Andersen, D., C. C. Kinze, and J. Skov. 1992. The use of pelvic bones in the harbour porpoise
Phocoena phocoena as an indication of sexual maturity. Lutra 35:105-112.
Birkhead, T. R. and A. P. Møller, eds. 1998. Sperm Competition and Sexual Selection. Academic
Press, San Diego.
Brownell, R. L. and K. Ralls. 1986. Potential for sperm competition in baleen whales. Report of
the International Whaling Commission Special Issue 8:97-112.
Byrne, P., J. Roberts, and L. Simmons. 2002. Sperm competition selects for increased testes
mass in Australian frogs. Journal of Evolutionary Biology 15:347-355.
Connor, R. C., A. J. Read, and R. Wrangham. 2000. Male reproductive strategies and social
bonds. Pp. 247-269 in J. Mann, R. C. Connor, P. L. Tyack, and H. Whitehead, eds.
Cetacean Societies. University of Chicago Press, Chicago.
Curtis, H. and N. S. Barnes. 1989. Biology, 5th edn. Worth Publishers, New York.
Gatesy, J., J. H. Geisler, J. Chang, C. Buell, A. Berta, R. W. Meredith, M. S. Springer, and M. R.
McGowen. 2013. A phylogenetic blueprint for a modern whale. Molecular Phylogenetics
and Evolution 66:479-506.
Harcourt, A., A. Purvis, and L. Liles. 1995. Sperm competition: mating system, not breeding
season, affects testes size of primates. Functional Ecology 9:468-476.
Heske, E. J. and R. S. Ostfeld. 1990. Sexual dimorphism in size, relative size of testes, and mating
systems in North American voles. Journal of Mammalogy 71:510-519.
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Hosken, D. J. 1998. Testes mass in megachiropteran bats varies in accordance with sperm
competition theory. Behavioral Ecology and Sociobiology 44:169-177.
Hosken, D. J. and P. I. Ward. 2001. Experimental evidence for testis size evolution via sperm
competition. Ecology Letters 4:10-13.
Mesnick, S. L. and K. Ralls. 2009. Mating Systems. Pp. 712-719 in W. F. Perrin, B. Wursig, and J.
G. M. Thewissen, eds. Encyclopedia of Marine Mammals, 2nd Edition. Academic Press.
Panebianco, M. V., M. F. Negri, and H. L. Cappozzo. 2012. Reproductive aspects of male
franciscana dolphins (Pontoporia blainvillei) off Argentina. Animal Reproduction Science
131:41-48.
Parker, G. A. 1984. Sperm competition and the evolution of animal mating strategies. Pp. 1-60
in R. L. Smith, ed. Sperm Competition and the Evolution of Animal Mating Systems.
Academic Press, London.
Perrin, W. F. 1975. Variation of spotted and spinner porpoise (genus Stenella) in the Eastern
Tropical Pacific and Hawaii. Pp. 209. University of California Press, Berkeley, CA.
Perrin, W. F. 2014. World Cetacea Database. Accessed at
http://www.marinespecies.org/cetacea on 2014-04-15.
Ramm, S. A., G. A. Parker, and P. Stockley. 2005. Sperm competition and the evolution of male
reproductive anatomy in rodents. Proceedings of the Royal Society B 272:949-955.
Ridley, M. 2004. Evolution. Pp. 751. Blackwell, Malden, MA.
Simmons, L. W. and D. J. Emlen. 2006. Evolutionary trade-off between weapons and testes.
Proceedings of the National Academy of Sciences 103:16346-16351.
Slice, D. E. 2007. Geometric morphometrics. Annual Review of Anthropology 36:261-281.
8

Uhen, M. D. 2010. The origin(s) of whales. Annual Review of Earth and Planetary Science
38:189-219.

9

Chapter 2: The progressive reduction of the cetacean pelvic girdle
Pelvic bones in whales and dolphins are not useless vestiges. Although the gradual
reduction of the pelvic girdle and loss of the external hind limbs in cetaceans is one of the most
significant themes of their evolution (Fordyce and Barnes 1994; Thewissen 1998; Uhen 2007;
Uhen 2010), the attenuation of the pelvic bones to their current state belies an essential
function: the anchoring of genitalia and associated muscles (Struthers 1881; Delage 1885;
Ommanney 1932; Rommel et al. 2007). Additionally, the size and shape of pelvic bones exhibit
considerable variation within and across contemporary cetacean species (Figure 2.1). The
important role of cetacean pelvic bones in copulation, along with the observed patterns of
morphologic variability, suggest that these structures may evolve under the influence of sexual
selection. Understanding the manifestations of cetacean pelvic bones in modern species
requires a discussion of this group’s evolutionary history and the forces that drove the
progressive reduction of their hindlimb.
The mammalian order Cetacea is a monophyletic group comprising the modern whales
and dolphins and their extinct ancestors (Uhen 2010; Gatesy et al. 2013). Taxonomically, it is
divided into three suborders: Archaeoceti, the ancient whales; Mysticeti, the baleen whales;
and Odontoceti, the toothed whales. The earliest cetaceans were terrestrial and quadrupedal,
with robust hind limbs and pelvic girdles (Gingerich et al. 2001; Thewissen et al. 2001; Gingerich
2003; Thewissen et al. 2009). Shared derived characters (i.e., synapomorphies) uniting the early
whales with modern forms are located in the skull, with the dramatic transformation of the
body and limbs associated with modern whales and dolphins appearing at various later stages
10

of cetacean evolution (Uhen 2010; Gatesy et al. 2013). The cranial synapomorphies of the early
cetaceans include: a long, narrow post-orbital region of the skull (Thewissen et al. 2007); a
thick, heavy (i.e., pachyosteosclerotic) auditory bulla with a large involucrum and sigmoid
process (Geisler and Luo 1998; Luo and Gingerich 1999; Thewissen and Bajpai 2001); incisors
and canines in line with the cheek teeth (Uhen 2007); lower molars lacking trigonid and talonid
basins (Thewissen et al. 2007); and cheek teeth adapted for shearing with re-entrant grooves
on the anterior margins of the molars (O'Leary and Uhen 1999). The progressive reduction of
the hindlimbs and pelvic girdle began with the transition from terrestrial to amphibious to fully
aquatic cetacean, and is documented in an exceptional fossil sequence. The dramatic transition
occurred in a period of 10-12 million years in the Eocene (Uhen 1998).
Among the earliest whales are the Pakicetidae, a group from the latest early to early
middle Eocene, that retained many apomorphic features of terrestrial artiodactyls, including: a
small mandibular foramen and mandibular canal (Bajpai and Gingerich 1998); long cervical
vertebra; long, gracile limbs with a double-pulley astragalus in the ankle; long metapodials; and
4 solidly fused sacral vertebrae (Thewissen et al. 2001). The derived cetacean-like characters of
pakicetids include a pachyosteosclerotic auditory bulla as well as other cranial features noted
above. Postcranial characters that might indicate the extent of aquatic-ness and the mode of
feeding have been interpreted broadly, but in describing the sacrum, the innominates, and the
long and slender leg bones of Pakicetus, Thewissen et al. (2001) interpreted them as “running
and jumping mammals” and not very efficient at swimming. Nevertheless, isotopic evidence
demonstrates that pakicetids spent a great deal of time in the freshwater environment,
drinking freshwater and eating freshwater prey (Clementz et al. 2006).
11

A second group of ancient whales, the Ambulocetidae, are known from the early middle
Eocene. They were also quadrupedal and possessed a complete pelvic girdle and hind limbs, but
the morphology of the axial and appendicular skeleton indicates that Ambulocetus was
amphibious, walking on land but using pelvic paddling and undulation in the aquatic
environment (Madar et al. 2002). Some ambulocetids have been interpreted as being ambush
predators instead of fast pursuit predators like modern cetaceans due to possessing with
dense, heavy bones (Thewissen et al. 1994).
Also from the middle Eocene are a third group of archaeocetes, the Remingtonocetidae.
They are characterized by long bodies with short limbs, and long skulls with long mandibles
fused as far back as the cheek teeth (Uhen 2010). With long, low bodies; strong, powerful tails;
and elongate jaws, remingtonocetids have been described as mammalian analogs to crocodiles
(Thewissen and Bajpai 2009). They likely walked on land as well as swam in the water
(Thewissen and Hussain 2000), and both sedimentological and isotopic evidence support an
amphibious but fully marine near-shore existence. Initial isotopic evidence supported a marine
diet for Danalistes (Clementz et al. 2006), but other taxa in the Remingtonocetidae have yet to
be analyzed isotopically.
The most derived of the semi-aquatic archaeocetes are the Protocetidae, which, based
on the locations of fossil discoveries, originated in the Indo-Pakistan region during the early
middle Eocene and rapidly diversified and spread to North Africa, Europe, North America, and
western South America (Uhen 2010). Their wide distribution and ability to colonize the oceans
of the world implies they were strong swimmers (Bajpai et al. 2009). All protocetids have been
12

found in coastal marine deposits, and all protocetids for which hind limbs are known had large
pelvic bones and femora, suggesting that they could likely walk on land as well as swim (Uhen
2010). Among the described protocetid genera is Georgiacetus from the southeastern United
States (Hulbert 1998; Hulbert et al. 1998), whose fossils date from approximately 40 million
years ago. Although hind limb elements are missing, Georgiacetus had large pelves with
prominent acetabulae, indicating the presence of large hind limbs, but the pelvic girdle was not
fused to the vertebral column (Hulbert 1998). Lacking a bony connection to the vertebral
column, the hind limbs of Georgiacetus likely could not support body weight for land-based
locomotion (Uhen 2008).
Basilosaurids were probably the first fully aquatic cetaceans, and thus represent an
important transition between archaeocetes and modern whales. Having highly reduced hind
limbs and flipper-shaped forelimbs, they were obligatorily aquatic (Gingerich et al. 1990; Uhen
1998, 2004). Superficially resembling modern whales, basilosaurids lacked some features
associated with modern species such as baleen or echolocation, but nonetheless possessed
many shared derived characters linking them with their modern counterparts.
Recognizing the important synapomorphies between Basilosauridae and Neoceti
(modern cetaceans), Uhen (2008) defined a new clade, Pelagiceti, which includes Basilosauridae
+ Neoceti. Among the diagnostic characters for Pelagiceti are: greatly reduced pelvis and pes,
along with rotation of the pelvis (Gingerich et al. 1990; Uhen and Gingerich 2001); higher
number of lumbar vertebrae; and rectangular, short, dorsoventrally compressed caudal
vertebrae (Uhen 1998, 2004). Although basilosaurids had external hind limbs, they were
13

extremely reduced in size and the pelves were completely dissociated from the vertebral
column. The hind limbs of basilosaurids could not, therefore, bear any significant weight on
land. Although too small to be involved in locomotion, Gingerich et al. (1990) proposed the
highly reduced external hind limbs in Basilosaurus may have had an accessory role in copulation
by acting as guides or otherwise making possible the grasping of mates. Others have
interpreted the diminutive external hind limbs as possibly aiding in locomotion in shallow water
(Fordyce and Barnes 1994), or as vestigial structures with no function (Berta 1994).

Pelvic bones in modern cetaceans
During the evolutionary transition from archaeocetes to modern whales, the gradual
reduction of the hind limbs was concomitant with a shift in the mode of locomotion (Bejder and
Hall 2002). The development of flukes—neomorphic outgrowths of skin and fibrous connective
tissue at the distal end of the body—was a major innovation in the evolution of cetaceans,
allowing a switch from drag-based propulsion produced by the limbs to vertical undulation and
lift-based propulsion (Fish 1996, 1998; Fish et al. 2006). The undulatory propulsion of cetaceans
generates high levels of thrust on both the upstroke and downstroke. There is no recovery
phase, so propulsion is produced throughout the stroke cycle (Williams 2009). One possible
explanation for the elimination of functionless, drag-inducing external hind limbs so early
cetacean evolution is the increased hydrodynamic and kinematic efficiencies resulting from a
switch to lift-based propulsion from the less efficient drag-based swimming.
14

Gatesy et al. (2013) recognize two major steps in the reduction of hind limbs: 1) great
reduction in the size of the limb occurring 48-42 mya, as observed in the protocetids and
basilosaurids; and 2) loss of distal elements and incorporation of any remaining elements into
the body wall, occurring approximately 41 mya in the unknown ancestors of modern
Odontoceti and Mysticeti. While variable in manifestation, mysticetes usually possess
internalized vestigial leg bones in the form of bony or cartilaginous femora and/or tibiae in
addition to the paired pelvic bones. In contrast, odontocetes usually have only paired pelvic
bones (Figure 2.2). The only odontocete to typically possess vestigial hind leg elements is the
sperm whale, Physeter macrocephalus (Berzin 1972); nevertheless, there are documented
instances of atavistic hind limbs in several cetacean taxa. Atavisms refer to the reappearance of
ancestral characters in individual members of a species that remind us that the genetic and
developmental information originally used in the production of such characters have not been
lost during evolution, but instead still lie within the genome and in the process of embryonic
development (Hall 1995).
A recent striking case of atavism in a bottlenose dolphin (Tursiops truncatus) shows two
sets of flippers: an anterior pair placed in the normal position, and a posterior pair in the region
of the pelvic girdle (Ohsumi 2008). Although uncommon, similar cases of atavistic hind limbs
have been reported in at least two other dolphin genera: Delphinus (Sleptsov 1963), and
Stenella (Ogawa 1953; Ohsumi 1965). Externally visible atavistic hind limbs seemingly occur
more commonly in cetacean taxa that typically retain internal hind limb elements in addition to
pelvic bones. Andrews (1921), for example, described external hind limbs in a humpback whale
(Megaptera novaeangliae). In a review of atavistic hind limbs in sperm whales (P.
15

macrocephalus), Nemoto (1963) reported the prevalence of atavism as 0.02% (i.e., 1 in 5,000
individuals).
Atavistic hind limbs in cetaceans apparently result from a mutation that prolongs limb
bud development (Bejder and Hall 2002). Early in the development of the cetacean embryo,
both forelimb and hindlimb buds are visible. By about the fifth week of development, while the
forelimbs go through a period of extended development that results in hyperphalangy in the
flippers (Cooper et al. 2007), the hindlimb buds begin to regress (Sedmera et al. 1997; Bejder
and Hall 2002; Thewissen et al. 2006). Flipper hyperphalangy and hind limb reduction, both
features of the fast-swimming body plan in cetaceans, may represent opposite extremes of
embryonic pattern heterochrony in limb development (Richardson and Oelschläger 2002).
Minor disruptions of those heterochronic patterns may result in anomalous atavisms.
During embryonic limb bud development, the outer edge of the bud has a thickened
external layer of ectoderm, called the apical ectodermal ridge (AER). Cascades of many
different genes are involved in patterning the limb and establishing the axes, and any disruption
of this cascade results in a failure to express the proper genes later in the sequence. A study of
spotted dolphin embryos (Stenella sp.) demonstrated that the hind limb bud initially has a
functional AER, but at a certain point the Fgf8 gene ceases to be expressed, resulting in a failure
of the AER to be maintained and causing the hind limb bud to degenerate (Thewissen et al.
2006). According to Hall’s definition of rudimentary and vestigial structures (Hall 2003), limb
buds in cetacean embryos are rudiments but the hind limb skeletal elements found in adults of
those same taxa are vestiges because modern whales and dolphins evolved from ancestors with
16

hind limbs and because homologous structures (limb buds and hind limbs) are found in closely
related groups.

The nature of vestigial structures
Vestigiality in its various forms provides evidence for biological evolution. Although the
term vestigial was not introduced until much later (Wiedersheim 1893), Darwin was keenly
aware of the concept and included in Origin of Species (Darwin 1859) and Descent of Man
(Darwin 1871) extensive catalogs of rudimentary organs in humans to support his reasoning for
the concept of natural selection. The implication was that vestigial structures are non-
functional and presumably non-adaptive: over time vestigial structures will degenerate if they
do not confer a significant enough advantage in terms of fitness to avoid the effects of genetic
drift or competing selective pressures. If not on an evolutionary trajectory of disappearing
entirely, vestigial structures are at a minimum selectively neutral.
As characterized by Futuyma (1998), vestigial structures formerly served a function in a
descendant species’ ancestors but no longer have that function. Common examples include
flightless insects with non-functional wings concealed beneath a fused wing cover (rendering
the wings useless), and blind cave-dwelling organisms that possess various stages of degenerate
eyes. In a more nuanced definition, Hall (2003) makes a distinction between rudiments and
vestigial structures. Rudiments are partly formed or incomplete transformations of a
developmental feature and therefore are only present in the embryonic stage. Vestigial
17

structures, on the other hand, are present in adult forms and are defined as evolutionary
remnants (or historical relics) of an ancestral feature.
Assessing the lack of function in vestigial structures is problematic and necessitates a
thorough understanding of an organism’s biology. For example, the wings of flightless birds like
the emu may no longer have a function in powered flight, but those same wings are
nevertheless important in balance and communication (Hall 2003). Similarly, flightless
cormorants and penguins use their wings for underwater propulsion. In these examples, the
“vestigial” wings have contemporary uses quite different from their original function and are
more properly recognized as exaptations (Gould and Vrba 1982).
The reduced pelvic bones in living whales and dolphins are often described as vestigial
structures (Feldhamer et al. 2003; Gatesy et al. 2013), and even as “useless vestiges” (Curtis
and Barnes 1989). Although correct in the sense that presence of a reduced pelvic girdle in
extant cetaceans is a relic of their quadrupedal ancestry, calling the pelvic bones of cetaceans
“vestigial” commonly leads to a misinterpretation of their functional significance. The human
vermiform appendix, for example, is frequently cited as a functionless vestige of the cecum that
formerly had an important role in the digestive tract of human ancestors. However, Bollinger et
al. (2007) recently showed the appendix retains a secondary function in the human immune
system. The pelvic bones of living cetaceans fall into the same category of having lost one
functional role but retaining another one.

18

Pelvic bones have a function
Although the reduced pelvic bones in modern cetaceans no longer have a significant
role in locomotion, they retain their function as anchors the genitalia and associated muscles
(Delage 1885; Struthers 1889; Abel 1907; Meek 1918; Anthony 1922; Slijper 1966; Rommel et
al. 2007). It has also been suggested that cetacean pelvic bones support abdominal muscles
(Arvy 1976, 1979; Pabst et al. 1998) and muscles associated with defecation (Simoes-Lopes and
Gutstein 2004). The penis is anchored to each of the paired pelvic bones by paired crura which
coalesce distally to form the main body of the penis (Rommel et al. 2007) (Figures 2.3, 2.4). The
ischiocavernosus muscles, also associated with the pelvic bones, are robustly developed in all
cetaceans (Ommanney 1932). In the harbor porpoise, the paired ischiocavernosus muscles
attach to and entirely surround the pelvic bones (Meek 1918). The same arrangement is found
in the common dolphin (Fig. 2.5). In the mesoplodont beaked whales, Anthony (1922) described
the ischiocavernosus as having double origins: along the entire length of the pelvic bone and
also from an aponeurosis posterior to the pelvic bone. Among baleen whales, Daudt (1898)
places the ischiocavernosus at the “hinteren” (back) of the pelvic bone (Fig. 2.3).
Delage (1885) speculated that the paired ischiocavernosus muscles acted independently
to pull the penis to one side or the other during copulation. Ommanney (1932), on the other
hand, dismissed this as implausible because he considered the ischiac attachment of the
ischiocavernosus muscles to be inadequate for this kind of action. According to Ommanney the
immense mass of muscle is mostly confined to the face of the corpus cavernosum and
therefore most likely has a compressor action upon the corpus cavernosum. In his discussion,
19

Ommanney (1932) struggled with the true function of the ischiocavernosus muscles. Do they
cause the penis to become tumescent by compressing the proximal portion of the penis and
forcing the blood to the distal portion? Or could they possibly control movement of the penis
during copulation? He chose the former explanation based on the small portion of the muscle
he observed attaching to the pelvic bones. However, Ommanney’s dissections also show the
ischiocavernosus muscles extending deeply like fingers into the base of the penis (Figure 2.4;
Ommanney 1932). It seems plausible that the dexterous maneuverability observed in the penis
of cetacean males (e.g., Mate et al. 2005) might be a result of controlled contractions of the
paired ischiocavernosus muscles.

The structure of cetacean pelvic bones
In most tetrapods, including terrestrial mammals, the innominate consists of three
fused bone elements: the ischium, the ilium and the pubis (Romer and Parsons 1977). These
independent elements each have a unique ossification center as they develop in the fetus,
eventually fusing to become a single solid bone. The three elements merge at the acetabulum,
the cupped socket that articulates with the head of the femur. The paired left and right
innominates comprise the pelvic girdle, fusing ventrally at the pubic symphysis and articulating
with the sacral vertebrae dorsally. In addition to supporting the bones of the hind limbs, the
innominates of tetrapods are the origin for muscles associated with locomotion as well as
muscles that support the genitalia (Gray 1901).
20

In modern cetaceans, the structure of the innominates has been radically modified in
size, shape, and relative position. Among the odontocetes, the innominates consist of a pair of
small, rod-shaped structures with no articulation with the axial skeleton (i.e., the vertebral
column). In contrast, the mysticetes, or baleen whales, possess pelvic bones that are typically
crescent or boomerang-shaped, but are also dissociated with the vertebral column. The named
elements that comprise the cetacean pelvic bones have yet to be confirmed despite receiving
much attention from researchers. Their identification has been confounded because
comparative anatomists use muscle attachment sites to determine homologous bones in
disparate taxa. The soft tissues in the pelvic and caudal region of cetaceans, however, are highly
derived and proper identification of homologous muscles therefore continues to be
problematic.
Yablokov (1974) considered it possible to clearly distinguish the boundaries between the
pubis, ilium and ischium in the cetacean pelvic bone, but at the same time acknowledged that
such distinction is usually difficult. In all mammals, the paired ischia are the sites of origin for
the paired ischiocavernosus muscles. Using the principal of homology, the portion of remnant
pelvic bone that is the site of origin for the ischiocavernosus muscle can be identified as the
ischium. In mysticetes it appears the pelvic bone may consist of the 3 ancestral elements
(Cuvier 1823; Abel 1907). Certainly, the ischiocavernosus muscles are anchored only to the
posterior portion of the mysticete pelvic bones (Figures 2.3,2.4; Daudt 1898; Ommanney 1932).
In an early analysis of the harbor porpoise (Phocoena phocoena), a toothed whale, Abel (1907)
proposed the ilium and ischium together comprise the pelvic bone. Tajima et al. (2004),
however, based on the relationship of the pelvic bones to the surrounding soft tissues in the
21

finless porpoise (Neophocaena phocaenoides), identified the pelvic bones in that species as
comprising the fused remnants of the pubis and ischium. Simoes-Lopes and Gutstein (2004)
established that the paired ischiocavernosus muscles originate on the paired pelvic bones of
the three species they examined, Pontoporia blainvillei, Tursiops truncatus, and Sotalia
guianensis, thus confirming at a minimum that the ischium is a component of innominate in
those species. That conclusion corresponds to the earlier determination of previous authors
(Eschricht and Rheinhart 1866; Flower 1876; Howell 1930; Hosokawa 1951). Contrary to these
findings, Lönnberg (1938) described the pelvic bone of a Stenella attenuata specimen, noting
the presence of all 3 ancestral his observation of identifiable sutures, a finding that was not
previously described nor has since been replicated. Simoes-Lopes and Gutstein (2004)
suggested the occurrence of sutures in Lönnberg’s specimen might be a case of spontaneous
atavism, but nevertheless acknowledged that other authors (Cowan 1939; Omura 1957) also
established that the pelvic bones represent the ilium, ischium and pubis are fused into a single
bone in cetaceans. Importantly, Cowan (1939) was describing a fin whale (Balaenoptera
physalus) and Omura (1957) was describing a minke whale (B. acutorostrata), both of which are
mysticetes.
Arvy (1979) was unable to identify pelvic bones in fetal specimens using x-rays and
curiously proposed that cetacean pelvic bones are homologous with the epipubic bones of the
unrelated marsupials. Notwithstanding Arvy’s analysis, at a minimum the ischium comprises the
pelvic bone in odontocetes, while the ancestral condition of the pelvic bone consisting of
ischium, ilium and pubis seems to apply for mysticetes.
22

In discussing hind limb anatomy in cetaceans, Adam (2002) states that retention of the
pelvic bone is associated with attachment of the penis retractor muscle. Similarly, Thewissen
(2002) states that the main purpose of the cetacean pelvic bone “is the attachment of the
retractor penis.” Both Adam and Thewissen commit an error of synonymy, which unfortunately
has been repeated in the literature (e.g., Gatesy et al. 2013). A synonym for the
ischiocavernosus muscle is erector penis muscle, which due to similarity to “retractor” may be
the source of error in Thewissen (2002) and Adam (2002). In fact, the retractor penis muscle
has no contact with the pelvic bones but instead “takes origin from the wall of the rectum
immediately posterior and dorsal to the bulbus” and is “inserted into the preputial fold”
(Ommanney 1932). The retraction of the penis is brought about solely by the action of these
muscles, such that in their retracted state the muscles retain the length of the penis within the
genital fold (Figure 2.4).
The retracted penis is bent, forming a sigmoid curve within the genital slit (Daudt 1898;
Kükenthal 1909; Slijper 1973; Slijper 1979). Rommel et al. (2007) describe the retractor penis as
originating on the superficial surface of the rectum and attaching to the ventral surface of the
penis just distal to the sigmoid flexure. In some cases, the cetacean retractor penis muscle has
been reduced to merely a ligament (Rommel et al. 2007). The contracted retractor penis muscle
apparently maintains the position of the non-erect penis within the prepuce, although Slijper
(1966) proposed that it might function as “a brake in regulating the stretching of the penis
during erection.” In form and function, the cetacean penis is very similar to that of artiodactyls.
Flower (1883a, b) noted this affinity in his early attempt to classify cetaceans with the
artiodactyls. In cetaceans, the non-erect position of the fibroelastic penis is curved into a
23

sigmoid flexure within the body wall, as is seen in ruminants. When the retractor muscles are
relaxed, the penis becomes “erect” although not through the influx of blood into spongy tissue,
but rather through the elasticity of the penis.

Summary
The earliest cetaceans were land mammals from approximately 54 million years ago in
the early Eocene (Uhen 2010). A rich fossil record provides remarkable evidence of the
evolutionary transition from a quadrupedal and terrestrial mode of existence to a fully aquatic
one. Among the dramatic adaptations to a specialized marine existence were features that
increase hydrodynamic and kinematic efficiency: telescoping of the skull, hyperphalangy of the
forelimb, development of flukes and robust axial muscles for propulsion, and reduction of hind
limbs to reduce drag. In living genera of whales and dolphins, external hind limbs are absent
except in the rare occurrences of atavisms. Examples of atavistic hind limbs, along with the
brief development of hind limb rudiments in embryos of dolphins, provide ontogenetic data to
support the fossil record of the terrestrial ancestry of modern cetaceans. Only dramatically
reduced hind limb elements hidden within the body wall remain in living forms. Among the
baleen whales, the paired pelvic bones are dissociated from the vertebral column and are often
accompanied by small vestiges of the femora, and more rarely, the tibiae. In most of the
toothed whales, on the other hand, all that remains of the pelvic girdle is a pair of reduced
pelvic bones that are dissociated from the vertebral column. The highly reduced nature of the
pelvic bones and the obvious absence of their former role in terrestrial locomotion have led to
24

the common assumption that they are useless vestiges on an evolutionary trajectory of being
entirely lost (Curtis and Barnes 1989). However, pelvic bones in cetaceans, as in other
mammals, have a secondary role in supporting the genitalia and associated muscles. The
significant function of pelvic bones in mating has led to the persistence of these “vestigial”
structures in cetaceans despite 40 million years of a legless, entirely aquatic mode of life.
Furthermore, the reproductive role of pelvic bones has important implications in their
variability in size and shape, aspects of which will be explored in subsequent chapters.
25

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Figure 2.1. Paired pelvic bones from several odontocete species, showing interspecific variation
and bilateral asymmetry. Top row (left to right): LACM 72591 Phocoena phocoena (harbor
porpoise); LACM 84284 Lagenorhynchus obliquidens (Pacific white-sided dolphin); LACM 97204
Delphinus capensis (long-beaked common dolphin); LACM 84251 Phocoenoides dalli (Dall’s
porpoise); LACM 85952 Stenella coeruleoalba (striped dolphin). Bottom row (left to right):
LACM 27074 Inia geoffrensis (Amazon River dolphin); LACM 54012 Pontoporia blainvillei
(franciscana); LACM 86041 Neophocaena phocaenoides (finless porpoise); LACM 84252 Feresa
attenuata (pygmy killer whale); LACM 84083 Mesoplodon carlhubbsi (Hubb’s beaked whale).
36

Figure 2.2. Remnant hind limb structures in modern cetaceans. A. Mysticetes, such as the Right
Whale (Eubalaena sp.) typically possess bony and/or cartilaginous vestiges of the femora and
tibiae associated with the paired pelvic bones. B. On the other hand, the normal state for
Odontocetes such as the common dolphin (Delphinus sp.), is to have only the paired pelvic
bones.

37

Figure 2.3. Penis of a gray whale, Eschrichtius robustus, attached to the two pelvic bones (WFS
1034; photo archives of Natural History Museum of Los Angeles County). The main body of the
penis forks into two crura, each of which anchors to a pelvic bone. The two large
ischiocavernosus muscles (mostly removed in this dissection) encapsulate the proximal portions
of the right and left crura and also originate on the surface of the pelvic bones.
38

Figure 2.4. Penis and associated structures of a fin whale, Balaenoptera physalus (adapted from
Ommanney 1932). Note the crus of the corpus spongiosum does not anchor to the pelvic bone.
a. Terminal cone of penis
b. Retractor penis muscle (cut)
c. Corpus spongiosum urethrae
d. Shaft of corpus spongiosum penis
e. Pannicular sheath of penis
f. Ischiocavernosus muscle
g. Crus corpus cavernosum
h. Triangular ligament
i. Pelvic bone
j. Bulbocavernosus muscle
k. Rectum

39

Figure 2.5. Penis and associated structures of long-beaked common dolphin, Delphinus
capensis. The dissection shows the paired pelvic bones and their close association with the
paired ischiocavernosus muscles. The main body of the penis, the corpus spongiosum,
bifurcates into two crura (hidden within the ischiocavernosus muscles), each of which anchors
to a pelvic bone on the medial side. The retractor penis muscle keeps the penis positioned
inside the genital slit until it is relaxed during copulatory behavior. The retractor penis muscle
does not originate on the pelvic bones, as is reported in some recent references.

40

Chapter 3: Comparing Cetacean Pelvic Bones: Challenges and Solutions

This study represents the first comprehensive quantitative analysis of pelvic bones
across modern cetaceans. One major obstacle to an earlier investigation of this nature has been
the scarcity of specimens. Cetaceans are rare in systematic collections due to the logistical
difficulty and expense in acquiring, preparing, storing and maintaining large aquatic mammal
specimens. Moreover, the protected status of most cetacean species requires that specimens
acquired in the past 40 years have been collected opportunistically, typically by the salvage of
stranded carcasses by authorized institutions or individuals. As a result, fewer than a dozen
museums in the world have more than 1,000 marine mammal specimens in their collections
(Heyning 1991; Heyning and Mead 2009). Within those collections, pelvic bones are rarely
collected and curated due to their relatively small size and their dissociation from the rest of
the skeleton. Of the nearly cetacean 10,000 specimens evaluated for the current study, less
than 3% included pelvic bones and fewer than that were from sexually mature specimens.
Another challenge until now has been the absence of appropriate analytical methods.
Pelvic bones from cetaceans are devoid of distinguishing landmarks, precluding the use of
traditional morphometric techniques for comparative analyses. More specifically, cetacean
pelvic bones lack readily identifiable features such as suture lines, foramina, or protuberances
that are traditionally used as homologous landmarks between specimens. As a result,
determining which ancestral elements comprise the cetacean pelvic bone remains unresolved.
The ischium, ilium, and pubis bones comprise the typical tetrapod innominate (Romer and
41

Parsons 1977), but which of these three bones form the cetacean pelvic bone has yet to be
determined (Rommel et al. 2007; see also discussion in Chapter One).
Classic accounts of cetacean pelvic bones were entirely descriptive treatments (e.g.,
Struthers 1881, 1889; Abel 1907; Lönnberg 1910) that lacked robust quantitative
methodologies. Even relatively recent analyses (van Bree 1973; Andersen et al. 1992) used
simple measurements such as total length and total weight as distinguishing characters among
pelvic bones, unfortunately ignoring the complex but more biologically informative features
that describe shape. Traditional morphometrics applies multivariate statistical analyses to sets
of morphological variables to describe patterns of shape variation within and among specimens
(Adams et al. 2004), but require a sufficient number of landmarks that are homologous across
specimens being compared. Robust statistical methodologies to analyze complex objects
deficient in homologous landmarks have recently been introduced (e.g., Gómez-Robles et al.
2013) providing a novel approach to the analysis of complex objects like pelvic bones.
The methods comprising landmark-based geometric morphometrics quantify the overall
shape of anatomical objects using the coordinates of homologous locations from those objects
and subsequently use sophisticated statistical analyses to describe and compare shape
variation (Bookstein 1991; Adams et al. 2004; Zelditch et al. 2004). Importantly, these
techniques take advantage of recent developments in 3-dimensional imaging technologies,
which capture points along the entire surface of anatomical structures, objectively providing
more complete descriptions of those structures. With data from surface scans, both landmarks
and semi-landmarks can be used for more comprehensive descriptions of shape and facilitating
42

more rigorous quantitative comparisons of anatomical structures (Mitteroecker and Gunz 2009;
Serb et al. 2011). Landmarks are coordinates of homologous locations on different objects,
whereas semi-landmarks may not homologous, but instead include point coordinates along the
surface of the objects that closely capture their surface topology (Gunz et al. 2005;
Mitteroecker and Gunz 2009).

Specimens
An initial survey for pelvic bones in the cetacean collection at the Natural History
Museum of Los Angeles County established several factors that render the identification and
study of cetacean pelvic bones challenging. First, cetacean pelvic bones exhibit considerable
age and sexual variation, and are difficult to distinguish from the other osteological elements
comprising a complete disarticulated specimen in a box. In addition, there is dramatic variability
in pelvic bone morphology between species (Figure 1.1), so there is no universal search image
for “pelvic bone” across the entire group of whales and dolphins. Finally, simply distinguishing
side (i.e., left from right) and orientation (i.e., anterior from posterior; dorsal from ventral) was
nearly impossible when examining isolated specimens within a box. These challenges were
resolved with practice, experience, and dissection of fresh specimens.
Dolphin and whale carcasses acquired through the Natural History Museum of Los
Angeles County’s Marine Mammal Stranding Program provided the opportunity to dissect and
identify pelvic bones from several different cetaceans. More than 25 specimens comprising
male and female common dolphins (Delphinus sp.), bottlenose dolphins (Tursiops truncatus),
Cuvier’s beaked whales (Ziphius cavirostris), and fin whales (Balaenoptera physalus) were
43

dissected and examined. Pelvic bones were dissected away from associated soft tissues, then
cleaned and labeled with their correct orientation and side (left vs. right). Labeled bones were
used as an aid in identifying pelvic bones from specimens already in the collection. Eventually,
identification of pelvic bones, as well as side and orientation, was accomplished without the
need for comparative material.
A total of 254 paired pelvic bone specimens from 38 species of cetaceans were obtained
from museum collections, including 9 mysticete species and 29 odontocete species (Table 3.1).
For the current analyses, only specimens from adult individuals of known sex were used
(N=152, Table 3.1). Age was determined using published minimum body length for adults of
each species. When available from the same specimen, the left and right first vertebral ribs (i.e.,
anterior-most ribs articulating with the thoracic vertebrae) were used as controls because they
are not directly involved in reproduction and ostensibly their morphology is not influenced by
sexual selection as is hypothesized for pelvic bones. Moreover, the unique morphology of the
first vertebral ribs makes them quickly distinguishable from all other skeletal elements and easy
to locate in a boxful of disarticulated skeletal elements. Due to the large size of baleen whale
ribs, however, they were not included as controls in the analyses.

Three-dimensional laser scanning
All specimens were scanned using a NextEngine 3D Laser Scanner HD Model 2020i and
ScanStudio HD PRO version 1.3.0 software (NextEngine, Inc. and Shape Tools, LLC; Santa
Monica, CA) installed on a PC laptop running Windows 7. The portable desktop laser scanner
contains two arrays of four solid state lasers, two 3.0 megapixel cameras, and two integrated
44

lights for image capture, producing high resolution digital models with colorized textured
surfaces that can be overlaid on a mesh model of three-dimensional coordinates (Figure 3.2).
The scanning system includes a rotating AutoDrive platform with an object gripper that secures
the specimen being scanned 6.5 to 30 inches (16 – 76 cm) in front of the scanner, depending on
the size of the specimen being scanned. Smaller objects can be placed closer to the scanner.
Larger objects require a wider field of view and are accordingly placed further from the
scanner.
Optimal scanning of an object requires experimentation with software settings and
extrinsic factors, such as object positioning and ambient lighting. Table 3.2 lists the optimal scan
distances and scanner settings for specimens used in the current study. RANGE was set to
Macro, Wide, or Extended distance modes based upon the size of the bone being scanned. For
bones up to 10 centimeters long, the Macro range was used and bones were positioned
approximately 16 cm from the scanner. Bones 10 – 45 cm long were placed optimally 43 cm
from the scanner using the Wide range setting. For bones up to 60 cm long, Extended range was
used with the bone placed 76 cm from the scanner. Using Extended range scans required an
optional extension data cord and an upgrade to the HD PRO scanning software, both acquired
separately from NextEngine, Inc. (Santa Monica, CA). Pelvic bones from most dolphin species
were small enough (2-10 cm) to be scanned using the Macro setting, while the largest bones
processed (up to approximately 60 cm) were pelvic bones from baleen whales, which were
scanned using the Extended range setting. Range setting affects the resolution of the scans,
varying from 0.005 inches for Macro scans to 0.015 inches for Extended scans.
45

All specimens were scanned using 360 degree positioning, which scans an object from
every angle by rotating the scan platform between scans. In the 360 degree scan mode, the
number of Divisions is assigned to control the total number of scans and the degree of rotation
between scans. For example, setting Divisions to “10” results in 10 total scans performed at 36
degree intervals. Individual scans between rotations are grouped as a scan family for later
processing. Depending on a specimen’s idiosyncrasies, each bone was scanned using between
12 and 16 Divisions. A higher number of divisions involves a longer total scan time, but was
usually required to capture accurate scans of very small and/or very thin bones.
POINTS PER SQUARE INCH was set between 1,100 and 40,000 points per inch
2
. This
setting in particular was a choice between scan precision and scan time. Specimens that were
particularly thin or small typically needed to be scanned at higher resolutions (up to 40k points
per square inch with 0.05 inch triangles) to accurately capture the bone’s morphology. Scans at
the highest resolution can take several hours each and consume several gigabytes of memory.
As each scan model was ultimately down-sampled prior to morphometric analyses (i.e., the
number of coordinates comprising the model was reduced 10-fold or more), the goal with
scanning was to obtain a highly accurate 3D model in a reasonable amount of time. Most bones
could be scanned at lower precision settings with no compromise in scan accuracy or
resolution.
TARGET was set based on the color and shade of the specimen being scanned: the
Neutral setting was used for typical “bone colored” bones; the Light setting was used for bones
bleached white; and the Dark setting was used for bones heavily stained with lipids or
46

otherwise deep in shade. Very dark or shiny specimens were dusted with white talc powder
prior to scanning to reduce reflection and improve scan quality.
Once a scan family was completed, the resulting 3D mesh model was visually inspected
on the computer screen to ensure it accurately represented the specimen being scanned.
Imprecise scans or scans with missing data were repeated until a usable scan was obtained.
Bones with particularly complex morphologies occasionally had to be scanned multiple times
from different positions, with the resulting two or more scans stitched together using the
ALIGN feature in ScanStudioHD. When multiple scans of the same specimen were necessary, 3
alignment marks were placed on the bones to facilitate the alignment process. Alignment marks
consisted of colored stickers of 1/8 inch diameter. Two alignment markers were placed at the
distal ends on one side of the bone, and a third marker was placed at the mid-point but on the
opposite side of the specimen. In Alignment mode, the ScanStudio HD software program shows
a split screen with the two different scan families that are to be aligned and merged. To align
the two scan families, matching colored digital pins were dragged using the computer mouse
from their home position in the upper right of the screen to the appropriate alignment marks
on the two scanned images. Two versions of the same colored pins were dragged to the
matching alignment marks on the two scans. Mouse controls were used to rotate (left mouse
button) or zoom in and out (scroll button) the scan images to precisely locate the alignment
marks on the scan models and ensure the accurate placement of the alignment pins. After all
three pairs of alignment pins were attached to their corresponding positions on the scans, the
“Attach Scans” menu function was selected to merge the scan families into a single model.
47

Scans always contained extraneous geometric data that were removed using the TRIM
function in the ScanStudio HD software package. Extraneous scan data could be minimized by
dragging the cursor to form a rectangle around the region of interest prior to initiating a scan.
Even so, portions of the scan platform and the support bar were consistently captured in
addition to the target specimen and required trimming. Using the sharp end of a thumbtack or
pin to hold the bone in place about 1 centimeter above the scan platform made it easier to trim
non-specimen data captured in the scan. To trim extraneous data, the Circle, Square, and
Polygon tools in the TRIM function were used to highlight all unwanted areas, using the
computer mouse. Highlighted areas were subsequently removed using the Trim button on the
menu. Once all unwanted geometric data were removed from the model, the individual scans
comprising that model were stitched together using the FUSE tool and saved into a single 3D
file. The Simplify setting in the FUSE mode was left at the default value of 0.0025 inches, which
allowed minimal decimation of the mesh. Advanced settings under the FUSE mode were also
left at their default values (e.g., the Resolution Ratio was left at 0.9). Files were saved in .scn
format to archive the original mesh model and allow for further manipulation, if necessary,
using the ScanStudio HD software. All files were also saved as output files in .xyz format (simple
x-y-z coordinates with one coordinate per line) for downstream geometric morphometric
analyses and for manipulation in other 3-D imaging software, such as MeshLab
(meshlab.sourceforge.net).

48

Landmark Acquisition
All geometric morphometric and computational analyses were performed using the R
scientific computing environment (R Core Development Team 2012) and the Python
programming language (Rossum and Drake 2001). To facilitate correct anterior vs. posterior
orientation of the pelvic bone point cloud models prior to downstream analyses, one
coordinate at the anterior end of each 3D model was selected as a provisional landmark. Using
the DIGIT.FIXED routine in the R package GEOMORPH (Adams and Otárola-Castillo 2012), each
file was visually examined to determine polarity (i.e., anterior vs. posterior end) and a fixed
landmark was digitized at the anterior end (Figure 3.3), with the landmark coordinates saved in
an independent output file for each pelvic bone .xyz file. The DIGIT.FIXED routine uses the RGL
library, an implementation within R for drawing 3-dimensional points, lines and polygons that
makes possible the manipulation of 3D objects on a 2D screen (Murdoch 2001). It provides the
ability to rotate objects, as well as zoom in and out. The RGL library automatically handles
depth cues by changing colors and shadows, and fading out distant points, creating an illusion
of three-dimensionality on a two-dimensional display.
Alignment of each rib model was determined in a similar fashion, but because ribs
exhibit greater complexity in shape, a total of 3 temporary landmarks were assigned to each
rib: ventral position, head position, and center of the tubercle (the facet that articulates with
the first thoracic vertebra) (Figure 3.4).
Within the DIGIT.FIXED routine using the RGL library, computer mouse buttons control
manipulation of the mesh model on the computer screen to allow the precise selection of fixed
49

landmarks. Pressing the left mouse button while moving the mouse around controls rotation of
the mesh model. The scroll button zooms in and out of the mesh model. Holding down the left
and right mouse buttons together while moving the mouse allows panning of the mesh model
on the screen. Landmarks are selected using the right mouse button, with the selected
coordinate highlighted in red. Once a landmark is selected, the user is asked confirm or repeat
the selection. After the desired number of landmarks have been confirmed, an output file is
generated in a designated directory with “fixedlmcoords.nts” added as a suffix to the
specimen’s original file name.
Each high resolution scan resulted in a mesh, or point cloud, consisting of tens of
thousands of 3-dimensional coordinates. Using those point clouds as a starting point, the
surface of each bone was quantified by digitizing 962 semi-landmarks spaced evenly over the
surface, modifying the procedure outlined in Gunz et al. (2005) and presented in greater detail
below. A relatively large number of landmarks were chosen to ensure the textural information
of each bone’s surface was well quantified.

Method for transforming and defining landmarks on pelvic bones (Figure 3.5)
For each pelvic bone point cloud, the two points furthest apart (red spheres 1 and 3 in
the left panel) were established from the convex hull (Graham 1972; Jarvis 1973), and a z-axis
was drawn between them (red line). Next, the coordinate on the point cloud located furthest
away on a perpendicular line from the z-axis was determined (red sphere 2). The three points
were then transformed so that point 1 = 0,0,0, point 2 = +x,0,+z, and point 3 = 0,0,+z. The
50

coordinates from points 1 and 3 were used as type 1 landmarks in downstream analyses; point
2 was used to establish the semi-landmarks but was not itself used as a landmark.
Sixty evenly-spaced slices of points were then sampled along the z axis, where each slice
thickness was 0.5% the length of the z-axis. The right panel in Figure 3.5 illustrates the 30
th
slice
of points (black spheres) and the midpoint of the convex hull (green point in center). Moving in
increments of 22.5 degrees from the x-axis (only the first increment is shown in Figure 3.5), the
two closest points straddling the line connecting the midpoint (two points shown in blue, one
slightly obscured) were determined and a line was drawn to connect them (blue line). A semi-
landmark was defined as the intersection of the black and blue lines (green point) and was
named according to its slice (i.e., P30) and its angle (i.e., 22.5). In this fashion, 16 semi-
landmarks were calculated for each slice (360 22.5 ). Only the determination of semi-
landmark P30_22.5 is shown in detail; the other semi-landmarks are shown as green points
along the perimeter for completeness. A total of 962 landmarks (2 landmarks and 960 semi-
landmarks) were digitized for each pelvic bone. All other points from the original point clouds
were eliminated.

Method for transforming and defining landmarks on rib bones (Figure 3.6)
For the point cloud representing each rib specimen, three points were determined
using the method described for pelvic bones. Next, a fulcrum (black sphere) was placed at 1/3
the length of the z-axis, and the point cloud was divided into 60 slices of equal angle from that
51

fulcrum. The 30
th
slice (black lines and black points) is illustrated in the right panel of Figure 3.6
as a detailed example showing how semi-landmarks were assigned in ribs.
The small black points are the 3-D coordinates from the original scan. The centroid of
the convex hull of the 20% most medial points (blue sphere to left) and 20% most lateral points
(blue sphere to right) points were calculated and connected with a line segment (black line).
The medial-most and lateral-most coordinates closest to that line (via shortest distance) were
identified, then projected to fall exactly on the line (medial and lateral green spheres). The line
segment connecting the medial and lateral green spheres was then divided evenly (black
spheres) and lines perpendicular to the black spheres computed. All points from the original
scan within a certain distance to the perpendicular black lines were found, projected onto the
perpendicular line (not shown), and the midpoint computed (orange spheres on perpendicular
lines). Each orange sphere was then projected onto the plane parallel to the figure to find a
third point with which to draw a plane (indicated by orange triangles). The orange triangles
allowed the point cloud to be divided into anterior and posterior halves to account for complex
curvatures inherent in ribs. The corresponding green spheres on the perpendicular lines were
determined in the same manner as the lateral and medial green spheres, for a total of 16 semi-
landmarks for each of 60 slices through the rib. A total of 962 landmarks and semi-landmarks
were included in downstream analyses; all other coordinates from the original point cloud were
discarded.

52

Generalized Procrustes Analyses
All shape analyses were performed using the GPAGEN routing in the R package
GEOMORPH (Adams and Otárola-Castillo 2012). Using the set of landmarks and semi-landmarks
defined above, pairwise shape divergence among bones was quantified in a Generalized
Procrustes framework based on algorithms previously developed in Geometric Morphometrics
(Rohlf and Slice 1990; Bookstein 1997; Mitteroecker and Gunz 2009). Briefly, a Generalized
Procrustes Analysis translates the landmark coordinates to a common centroid (the center of
the shape), scales the coordinates to a centroid size of 1, then optimally rotates the set of
coordinates using a least-squares criterion until all the coordinates of corresponding landmarks
align as closely as possible (Bookstein 1991). The remaining Procrustes coordinates primarily
describe differences in shape while minimalizing the effects of size and orientation.
To improve alignment, the “landmarks” (technically semi-landmarks, according to
Bookstein 1991) were allowed to “slide” along the outline curve of the shape until they
matched as well as possible the positions of the corresponding points along the outline of the
reference specimen (Bookstein 1997; Adams et al. 2004; Gunz et al. 2005). The entire set of
pelvic bones were compared pairwise in this manner. In separate analyses, all ribs were also
compared pairwise. Prior to aligning, all left-sided bones were transformed into mirror-images
to match with their right-sided counterparts. The sum of the distance between aligned,
corresponding landmarks was taken as the shape distance, or Generalized Procrustes Distance
(GPD). The resulting multivariate data was then available for the standard statistical toolkit
used in morphometric analyses. Computations were run on the cluster of the USC Center for
High Performance Computing and Communications.
53

Technical replication
To validate scanning and computational precision, a subsample of 41 pelvic bones and
ribs were randomly selected and were scanned and analyzed multiple times. One pelvic bone
was scanned a total of 11 times, removing the bone from the scan platform each time before
replacing it in a slightly different position and rescanning using the same scan parameters.
Twenty different pelvic bones and 20 different ribs were each scanned twice, each time
removing the bone from the scan platform and replacing it before the second scan. By scanning
the same bones in different positions and subjecting the scans to downstream analyses, the
potential effects of positioning and distance from the scanner could be assessed. In all cases,
the shape differences calculated between replicates was less than 5% of the average pairwise
shape difference among all bones. Size differences of the scan replicates, quantified as the
median coefficient of variation (unbiased standard deviation/mean) for centroid size, was
0.0094 for pelvic bones and 0.0090 for ribs. Surface scanning using the three-dimensional laser
scanning, as well as the computational pipeline developed to quantify size and shape variances
in the bones, were highly repeatable.

Summary
Comparing anatomical features is the basis for understanding the evolutionary forces
that shape them. In the case of cetacean pelvic bones, the use of modern morphometric
methods to make robust comparisons has been hampered by the lack of definable landmarks
on those bones. This problem has been resolved using three-dimensional imaging for data
acquisition and novel, but rigorous, methods to analyze those data. The inclusion of surface
54

data generated by 3D imaging provides a richer description of overall shape than has been
previously available (Adams et al. 2004). The resulting high-resolution mesh is usually so dense
that it must be downsized, or “statistically thinned”, while still maintaining a maximum amount
of surface information. Direct analysis of the resulting coordinates as variables is not
appropriate because those coordinates still contain information about variation in size,
position, and orientation. Non-shape variation can be removed mathematically using
Procrustes methods, preserving only shape for subsequent statistical comparison.

55

Literature Cited
Abel, O. 1907. Die Morphologie der Hüftbeinrudimente der Cetaceen. Denkschriften der
Kaiserlichen Akadamie der Wissenschaften 81:139-195.
Adams, D. C. and E. Otárola-Castillo. 2012. Package 'geomorph': Geometric morphometric
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58

Figure 3.1. Digital models of a pelvic bone from a Dall’s porpoise (LACM 54420, Phocoenoides
dalli) produced by the NextEngine 3D Laser Scanner and visualized with MeshLab v1.3.0 mesh
processing software. A (top): Digital model with colorized surface texture overlay produced by
the laser scanner’s integrated digital camera. B (bottom): Digital model with surface overlay
turned off, showing the three-dimensional point cloud. Each dot represents a three-
dimensional coordinate with an independent x,y,z value.
59

Figure 3.2. Three-dimensional mesh model of the right pelvic bone from a long-beaked
common dolphin (LACM 96366, Delphinus capensis), with one fixed landmark (in red) chosen
using the digit.fixed routine in the GEOMORPH software package run in the R scientific
computing environment. The output after choosing the fixed landmark is (11.4476 -112.6771
33.4416), representing the x, y, and z coordinates respectively, of the landmark.

60

Figure 3.3. Three-dimensional mesh model of the right first vertebral rib from a long-beaked
common dolphin (LACM 96366, Delphinus capensis) with three fixed landmark (in red) chosen
using the digit.fixed routine in the GEOMORPH software package run in the R scientific
computing environment. The output after choosing the fixed landmarks is (23.6767 6.1986 -
11.2711; 43.7842 -113.869 -8.4031; 16.7714 -128.2144 -12.2783), representing the x, y, and z
coordinates of the 3 landmarks.
61

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Figure 3.4. Transforming and defining landmarks and semi-landmarks on pelvic bones. Left
panel: the two furthest points apart (red spheres 1 and 3) were found from the convex hull, and
a z-axis was drawn (red line). The point furthest away from that z-axis was found (red sphere 2).
All points were then transformed so that point 1=0,0,0, point 2=+x,0,+z, and point 3=0,0,+z. 60
evenly-spaced slices of points were sampled along the z axis, where each slice thickness is 0.5%
the length of the z-axis. Right panel: The 30
th
slice of points (black spheres). The midpoint of
the convex hull was calculated (green point in middle). Then, moving in increments of 22.5
degrees from the x-axis (only the first increment shown in detail), the two closest points
straddling the line connecting the midpoint (two points shown in blue, one slightly obscured)
was found and a line drawn connecting them (blue line). A landmark was defined as the
62

intersection of the black and blue lines (green point) and was named according to its slice (i.e.,
P30) and its angle (i.e., 22.5). Only P30_22.5 is shown in detail; the other green points are
shown for completeness. All other points were discarded for downstream analyses.

63

Figure 3.5. Transforming and defining landmarks on ribs. Left panel: All points were transformed
according to three points, as defined in Figure 3.4. A fulcrum (black sphere) was placed at 1/3
the length of the z-axis, and the bone scan was divided into 60 slices of equal angle from that
fulcrum. The 30
th
slice (black lines and black points) is shown as an example. Right panel: The
30
th
slice of points in detail. The small black points are the coordinates from the original scan.
The centroid of the convex hull of the 20% most lateral points (blue sphere to left) and 20%
most medial points (blue sphere to right) points were used to draw a line. The lateral/medial
point closest to that line (via shortest distance) was found, then projected to fall exactly on the
line (lateral/medial green spheres). The line connecting the lateral and medial green spheres
was divided evenly (black spheres) and lines perpendicular to the black spheres were
computed. All points from the original scan within a certain distance to the perpendicular lines
were found, projected onto the perpendicular line (not shown), and the midpoint then
64

computed (orange spheres on perpendicular lines). The orange sphere was then projected onto
the plane parallel to the figure to find a third point, with which to draw a plane (indicated by
orange triangles). Those orange triangles were used to divide the bone into anterior and
posterior halves and account for complex curvatures. The corresponding green spheres on the
perpendicular lines were determined exactly like the lateral and medial green spheres. Only the
green spheres are included in downstream analyses.

65

Table 3.1. Specimens examined. A total of 254 specimens from 38 cetacean species were
examined, including 9 mysticetes (baleen whales) and 29 odontocetes (toothed whales,
inclusive of dolphins and porpoises). Specimens were categorized as adults based on published
data.
Species total #
adult
males
adult
females
Mysticetes
Balaena mysticetus 6 0 0
Balaenoptera acutorostrata 4 1 1
Balaenoptera edeni 1 0 0
Balaenoptera musculus 8 1 1
Balaenoptera physalus 5 0 1
Eschrichtius robustus 4 1 0
Eubalaena australis 1 0 0
Eubalaena glacialis 2 1 1
Megaptera novaeangliae 4 0 0
Odontocetes
Delphinus capensis 36 26 3
Delphinus delphis 18 10 1
Feresa attenuata 5 2 0
Globicephala melas 2 0 1
Grampus griseus 6 4 0
Inia geoffrensis 5 2 0
Lagenorhynchus acutus 4 3 1
Lagenorhynchus obliquidens 5 4 0
Lissodelphis borealis 5 3 0
Mesoplodon carlhubbsi 2 0 1
Mesoplodon perrini 1 0 1
Mesoplodon sp. 1 0 0
Monodon monoceros 1 0 0
Neophocaena phocaenoides 2 0 0
Orcinus orca 2 1 0
Peponocephala electra 2 0 1
Phocoena phocoena 25 7 6
Phocoenoides dalli 10 6 0
Physeter macrocephalus 4 0 0
Pontoporia blainvillei 10 3 6
Pseudorca crassidens 1 1 0
Stenella attenuata 7 3 2
Stenella coeruleoalba 4 1 0
Stenella frontalis 1 1 0
Stenella longirostris 4 3 0
Steno bredanensis 5 4 0
Tursiops aduncus 2 1 0
Tursiops truncatus 47 21 13
Ziphius cavirostris 2 1 1
total specimens 254 111 41
66

Table 3.2. Optimal scan parameters. Specimen size dictated the scan settings as well as the distance
specimens were placed from the laser scanner. Positioning was always set at 360° to scan the surface of
specimens at every angle. Values uses for Divisions and Points per inch
2
varied according to the
idiosyncrasies of individual specimens, to optimize scan time versus scan quality. Higher values yielded
denser meshes but dramatically increased scan times. Values at the lower end for Divisions and Points
per inch
2
for produced high quality meshes for most specimens; thin bones and bones with complex
morphologies typically needed to be scanned at higher divisions and densities. Light, Neutral, or Dark
settings were used for Target depending on the darkness of the specimen.

Scanner Settings
Specimen size (in centimeters)
2 – 10 10 – 45 45 – 60
Range MACRO WIDE EXTENDED
Distance from scanner 16 cm 43 cm 76 cm
Positioning 360° 360° 360°
Divisions 12-16 12-16 12-16
Points per inch
2
10k - 40k 1.1k - 17k 1.1k - 17k
Target Light or Neutral or Dark
67

Chapter 4: Testes Evolution and Mating Strategies in Cetaceans
Very little is known of the mating ecologies of whales and dolphins. Observations of
their mating behavior in the natural environment are uncommon, and even direct observation
can be misleading when inferring mating strategies because, in many cetacean species, sexual
behavior is an important part of social interactions not directly related to reproduction (Kasuya
et al. 1993; Norris et al. 1994; Wells and Scott 1999). Moreover, mating ecology can vary within
taxa, especially those with wide-ranging distributions. Bottlenose dolphins (Tursiops sp.), for
example, have been shown to exhibit widely varying mating strategies in closely related species
as well as in different geographic populations of the same species. Male Indo-Pacific bottlenose
dolphins (Tursiops aduncus) in Shark Bay, Western Australia, form stable alliances of two or
three unrelated individuals that sequester and forcefully control the movements of individual
females (Connor et al. 1992b; Connor et al. 1992a). In contrast to this aggressive herding
behavior, the alliances formed by male common bottlenose dolphins (Tursiops truncatus) in
Florida establish temporary but non-aggressive “consortships” with females (Wells et al. 1987;
Wells and Scott 1999). Common bottlenose dolphins in other areas of the world have not been
shown to form similar male alliances. Because of these differences, neither direct observations,
nor taxonomic affinities are good predictors of mating ecology in cetaceans.
Evidence from testes evolution can shed light on this problem. A compelling body of
literature demonstrates a strong correlation between relative testes mass and mating strategy.
Theory predicts that males will increase their investment in sperm production as the level of
sperm competition increases (Parker 1970; Parker 1998). To the extent that size of testes is
68

correlated with the amount of sperm produced, there will be selection for larger testes under
conditions of intense sperm competition. Indeed, varying levels of sperm competition account
for variation in the relative size of the testes in a broad range of species exhibiting internal
fertilization (Gage 1994; Harcourt et al. 1995; Hosken 1997; Stockley et al. 1997; Hosken 1998;
Ramm et al. 2005; Firman and Simmons 2008).
The relationship between testes size and mating system is so strong in many mammal
groups that relative testes size is considered a credible indicator of mating system (Gomendio
et al. 1998). Males with small testes relative to their body size tend to participate in a single
male mating system with no sperm competition (e.g., monogamy or extreme polygyny, wherein
a single dominant male does all or most of the mating), while males with very large testes
relative to body size tend to experience intense sperm competition, as in a promiscuous mating
system (Table 4.1).
In a classic study assessing the relationship between testes mass and body mass among
a diverse sample of 133 species of mammals, Kenagy and Trombulak (1986) demonstrated a
significant positive correlation between the two (Figure 4.1). Additionally, they showed that
testes are small relative to body size in single-male breeding systems, and that testes are
relatively large in multi-male breeding systems. That analysis, however, included just 7
cetacean species: 5 toothed whales (odontocetes) and 2 baleen whales (mysticetes). Notably,
the testes of odontocete cetaceans stood out as the largest relative to body mass among all
mammals (Figure 4.1), with testes 7-25 larger than predicted for their body sizes (Kenagy and
Trombulak 1986). Meanwhile, the only two mysticete species included in the analysis had
69

testes masses just 19-23 percent of the predicted value for their body sizes. While the body
masses of odontocetes and mysticetes included in the study differed by three orders of
magnitude, the testes of the two groups were very close in absolute size (Kenagy and
Trombulak 1986). Due to the great disparities in relative testes size between the two groups of
cetaceans, as well as the small number of cetacean taxa examined, cetaceans were the only
major group in the analysis for which there was no detectable correlation between testes mass
and body mass. Patterns of variation in relative testes size among cetaceans and how they
relate to mating ecology remain largely unexplored.
Thus, the two major goals of this paper are to characterize variation in testes mass
across Cetacea and, based on testes detected variability, test predictions from sperm
competition theory. Characterizing variation in relative testes size has the potential to elucidate
mating ecology patterns in this charismatic but largely enigmatic group, particularly for cryptic
species that are infrequently encountered. Variation in testes mass results from sperm
competition and variance in mating success (Parker 1984; Birkhead and Møller 1998; Hosken
1998; Byrne et al. 2002). The largest relative testes sizes should be found in species with the
strongest sperm competition, for example, in species with promiscuous mating systems. In
contrast, the smallest relative testes sizes should be found in species with negligible or no
sperm competition. The latter category includes monogamous species as well as species with
strong polygyny, wherein a single male controls a harem. In monogamous mating systems a
single male is hypothetically the only male inseminating the female. Similarly, in a strongly
polygynous mating system, the dominant male prevents other males from mating with the
females in the harem. Thus, sperm competition is expected to be negligible.
70

Sperm competition theory also assumes that males have limited metabolic resources
with which to invest in reproduction, resulting in a trade-off between traits used in pre-
copulatory battles to gain mating opportunities and in post-copulatory traits used to ensure
successful fertilizations (Parker 1998; Simmons and Emlen 2006). It is predicted, for example,
that males investing in pre-copulatory structures, such as weapons or increased body mass
used to compete with other males in gaining matings, will have less energy to invest in post-
copulatory mating traits such as large testes which are advantageous in sperm competition
(Simmons and Emlen 2006). In other words, the presence of sexually dimorphic structures is a
useful indicator of the importance of pre-copulatory contest competitions between males for
access to females (Boness et al. 2002). Sexual dimorphism may take the form of body size
differences, presence of weapons, scarring, differences in body coloration and even courtship
behaviors. Fitzpatrick et al. (2012) demonstrated that testes mass is negatively associated with
investment in pre-copulatory weaponry in pinnipeds, a group of marine mammals that includes
the seals and sea lions. Similarly, it is expected that cetaceans with traits useful in pre-
copulatory contest competitions will correspondingly have relatively small testes.

Methods
Life history data were collected from the literature for 49 of the 92 (53%) currently
recognized species of cetaceans (Perrin 2014). Data collected included maximum body length
(cm), maximum body mass (grams), and maximum combined testes mass (grams). Length data
71

were most frequently available for most species, but body mass and testes mass data were
commonly unreliable and therefore not collected.
Testes mass data in the literature were often given as average values for a species. To
account for age and seasonal variation in testes size, however, only maximum values from
sexually mature males were used. Ideally, maximum values for testes mass came from sexually
mature males at the height of breeding season and therefore reflect the maximum sperm
production capacity for each species. This unfortunately ignores the fact that life history
parameters can vary sharply among different geographic populations of the same species
(Perrin and Reilly 1984), but the scarcity of available testes data made it necessary to use
maximum values for a species and not account for geographic variation in body size and
reproductive traits. Inaccuracies in the data available actually make conclusions drawn from
those data more conservative.
Another potential source of error in the data is that testes mass was inconsistently
reported with epididymes intact, epididymes removed, or the presence or absence of
epididymes not cited. Again, the maximum testes mass value reported in the literature was
used in the present analysis.
To account for organs increasing allometrically with body size, maximum body mass and
testes mass values were log- transformed before performing correlation and linear regression
analyses using the Linear Model (lm) function in the R statistical computing environment (R
Core Development Team 2012). MacLeod (2010) demonstrated that when percentage testes
mass was used instead of residual testes mass, the relative importance of sperm competition
72

was consistently overestimated in species with a body mass less than 200 kilograms, and
consistently underestimated in species with a body mass more than 200 kilograms. As a result,
using simple indices of relative testes mass, such as percentage of total body mass, to infer
levels of sperm competition is likely to lead to errors (MacLeod 2010). Accordingly, a best fit
linear model was calculated by standard regression of log body mass against log testes. The
resulting residuals, defined as the difference between actual values and fitted values along the
linear model, were used as the measure of relative testes mass for each species.
To test if the relationship between body mass and testes mass among cetaceans is the
same as the relationship reported for all mammals (Kenagy and Trombulak 1986), the
correlation coefficient (r), the slope, and the intercept of the two different linear equations
were compared. Using the procedure developed by Fisher (1921), each of the two correlation
coefficients were first transformed using the equation:

( )

[

]

(1)
Based on the transformed r values, the test statistic was calculated using Fisher’s z-test:

√

(2)
The significance of the difference between the slopes of the “cetacean only” and the “all-
mammal” equations was evaluated using Student’s t-test:

(3)
73

where

and

represent the slopes of the two equations and

is the standard error of
the difference between the two slopes.
To test the difference of the intercepts of the two equations, the pooled residual
variance was first calculated, where RSS 1 and RSS 2 are the residual sum of squares obtained
from each fitted linear model (Table 4.3):

(4)
Then the null hypothesis that the intercepts are identical (

) was tested using the
equation:

[

] (5)
where
1
and
2
are the means on the predictor variables of the two groups, “cetaceans” and
“all mammals” respectively. Finally, the test statistic was calculated using Student’s t-test:

(6)
To evaluate the intensity of pre-copulatory sexual selection, the occurrence of sexually
dimorphic traits were documented for each species. Sexually dimorphic characters included
weapons (e.g., tusks or teeth), sexual size dimorphism and behaviors such as singing. Weapons,
when present, are typically manifested in sexually mature males and indicate male-male
competition for access to females for mating. High levels of sexual size dimorphism are
associated with highly polygynous mating systems where the strength of pre-copulatory male-
male competition is elevated (Clutton-Brock et al. 1977). The presence of sexually dimorphic
74

traits was assessed against the framework of relative testes mass to test the idea of a trade-off
between the investment in pre-copulatory and post-copulatory mating strategies.

Results
Variation in residual testes mass suggests variation in sperm competition
The linear model showing the correlation between log maximum testes mass and log
maximum body mass in cetaceans is shown in Figure 4.2 (solid line, Y=0.2207X
0.5722
r
2
=0.58,
p<0.001). Testes residuals (Table 4.2) varied widely, ranging from -1.86 for the franciscana
dolphin (Pontoporia blainvillei), a species considered to be monogamous (Danilewicz et al.
2004; Panebianco et al. 2012), to 1.22 for the right whales (genus Eubalaena), baleen whales
known to engage in strong sperm competition (Brownell and Ralls 1986; Payne et al. 2001).
Other species with notably positive testes residuals include the dusky dolphin (Lagenorhynchus
obscurus, testes residual = 0.96), the short-beaked common dolphin (Delphinus delphis, testes
residual = 0.67), and the harbor porpoise (Phocoena phocoena, testes residual = 0.60). Although
testes residuals were used as measures of relative testes mass in the analyses, testes as a
percentage of body mass strikingly illustrates the energetic investment in testicular tissue. The
dusky dolphin, aptly nicknamed the “testicular dolphin”, has a maximum testes mass : body
mass ratio of 8.5% (van Waerebeek and Read 1994), while the maximum ratio of testes mass to
body mass in the “megatestes” harbor porpoise is 6% (Fontaine and Barrette 1997; Read 1999).
75

In contrast to the linear model for cetaceans, the relationship between log testes mass
and log body mass described for all mammal species by Kenagy and Trombulak (1986) had a
linear equation of Y=0.035X
0.72
. To illustrate the differences, the “all mammals” data, including
the fitted regression line, is plotted with the cetacean data (Figure 4.2). Many of the cetacean
species examined have plotted values above the “all mammals” line, indicating a strong general
trend of cetacean species possessing testes larger than would be predicted for mammals of
similar body masses. The cetacean data in the current analysis included 49 species across a
diverse spectrum of ecologies, and incorporated more refined data acquired over the past
three decades to the 7 species used in Kenagy and Trombulak (1986).
The statistical results of the two regression analyses (Table 4.3; only cetaceans from the
current study, and all mammals sensu Kenagy and Trombulak 1986) were used to compare the
correlation coefficients, as well as the slopes and intercepts of the two linear equations. The
correlation coefficient (r) for the “all mammals” analysis was 0.93; for the 49 species of
cetaceans analyzed separately, r was 0.75. The test statistic calculated using Fisher’s z-test
(Equation 2, above) was 3.81 (p = 0.0001) leading to rejection of the null hypothesis. Thus, the
correlation between testes mass and body mass in “all mammals” is significantly higher than
the correlation in cetaceans. In comparing the slopes, the “all mammals” model had a slope of
0.72 while the cetacean model had a slope of 0.57. Student’s t = 1.908 (p = 0.058, DF = 178),
leading to the conclusion that the two slopes are not significantly different. The intercept for
the cetacean only model was significantly higher than the “all mammals” model (t = 9.109; p <
0.0001, DF = 178).
76

Trade-off between weapons and testes
Interestingly, all cetacean species for which there is evidence of pre-copulatory sexual
selection had negative testes residuals (i.e., had relative testes sizes lower than would be
predicted for their given body masses) (Figure 4.3, Table 4.2). For example, among narwhals
(Monodon monoceros), only males possess tusks, used during intra-sexual jousting
competitions prior to mating (Silverman and Dunbar 1980; Best 1981). Narwhals have a testes
residual value of -0.51, indicating they have testes mass considerably smaller than would be
expected based on their body size. The enigmatic beaked whales (Family Ziphiidae) are also
sexually dimorphic: typically only males manifest one or two pairs of teeth which are used in
combat with other males. The most dramatic examples of this are exhibited in the genus
Mesoplodon. In the present analysis, Hubbs’ beaked whale (Mesoplodon carlhubbsi) has a
testes mass residual of -1.04, considerably below the regression line for cetaceans. Cuvier’s
beaked whale (Ziphius cavirostris) likewise has a testes residual of -0.30. On the other hand,
Baird’s beaked whale (Berardius bairdii) has a slightly negative testes residual of -0.04. Tellingly,
both males and females have erupted teeth in this particular species of beaked whale.
Some cetacean species don’t possess weapons, but nevertheless exhibit some form of
sexual dimorphism. These species also tend to possess relatively small testes. Expression of
sexual dimorphism within a species was determined from descriptions in the literature, and
included traits such as sexual size dimorphism (or SSD, where one sex is bigger than the other)
and body shape differences. Dall’s porpoise (Phocoenoides dalli, testes residual = -0.45), for
77

example, exhibits SSD, with adult males being slightly larger than adult females. Adult males,
however, also differ morphologically from females in having a strongly canted dorsal fin and a
prominent post-anal hump; features that have been associated with pre-copulatory sexual
selection (Jefferson 1990).
Another species with distinct and significant sexual dimorphism is the sperm whale
(Physeter macrocephalus, testes residual = -0.58), with mature male bulls measuring up to 50%
longer than mature cows (Berzin 1972; Jefferson et al. 2008). Fighting between males has rarely
been observed in male sperm whales, but the presence of head scarring implies that intrasexual
aggression occurs (Whitehead 2003).
Finally, the humpback whale (Megaptera novaeangliae), with a testes residual of -0.97,
exhibits several behaviors associated with pre-copulatory sexual selection. In addition to
producing complex songs ostensibly used to attract potential mates, male humpbacks engage in
aggressive intrasexual interactions while competing for access to females (Tyack and
Whitehead 1982; Baker and Herman 1984; Pack et al. 2002).

Discussion
The linear model presented here demonstrates a significant positive correlation
between maximum body mass and maximum testes mass in cetaceans (solid line in Figure 4.2;
r
2
=0.58, p<0.001). Additionally, there is wide variability in relative testes mass across species
and that variation is related to mating ecology. Right whales (genus Eubalaena), for example,
78

famously have testes that weigh nearly one ton (Omura et al. 1969), and based upon having a
large positive testes residual of 1.22, are predicted to engage in intense sperm competition
(Brownell and Ralls 1986; Payne et al. 2001). When a female mates with more than one male in
the same mating season, the sperm of those multiple males are competing to fertilize the one
available ovum. Direct observation of multiple male right whales mating with a single female
indicates they have a promiscuous mating system with elevated sperm competition (Mate et al.
2005). In the closely related bowhead whale (testes residual = 0.44), sexual activity often occurs
in large mating groups with “much whitewater as whales rapidly turn and spin around each
other, boisterously nudging and pushing” (Würsig and Clark 1993). At the opposite extreme is
the franciscana dolphin (Pontoporia blainvillei) with a testes residual of -1.86. The very low
relative testes size, along with lack of sexual dimorphism and external scarring, are strong
indicators that franciscanas are monogamous (Danilewicz et al. 2004; Panebianco et al. 2012).
The data presented also demonstrate that species with inferred pre-copulatory sexual
selection have small relative testes size. Male narwhals and beaked whales, for example,
manifest tusks or battle teeth used in aggressive bouts to establish dominance over rival males.
Similarly, male Dall’s porpoises, male sperm whales, and male humpback whales all exhibit
sexually dimorphic traits related to contest competitions for access to mates. All of the above
species have testes smaller than predicted based on their body size.
Emerging from these results is a negative relationship between investment in traits that
increase competitive ability in male-male contest competition (e.g., weapons and increased
body size) and investment in post-copulatory traits (increased testes mass, a proxy for sperm
79

competition). In other words, in cetaceans there is a trade-off in the pattern of investment in
pre-copulatory versus post-copulatory sexually selected traits, a pattern predicted in sperm
competition game theory (Parker et al. 2013).
That said, these strategies aren’t always mutually exclusive; one or more may be
operating simultaneously (Boness et al. 2002). As discussed above, male right whales
(Eubalaena sp.) have very large relative testes and engage in intense sperm competition
(Brownell and Ralls 1986). However, right whales also have rough skin patches called callosities
on their heads, on which barnacles accumulate, which in turn can be used as weapons against
other males. Scars from sharp barnacle shells are more common on males than females (Payne
and Dorsey 1983), suggesting inter-male aggression. Similarly, odontocetes such as Risso’s
dolphin and the pygmy sperm whale have moderately large positive testes residuals (0.56 and
0.58, respectively) but older males also tend to show rake marks along their heads (personal
observation), indicating some degree of direct intra-sexual aggression is operating in addition to
sperm competition.
Also of note is the general trend of cetaceans to exhibit much larger testes relative to
body size than mammals overall. A clear outlier in this regard is the dusky dolphin, with testes
comprising a remarkable 8.5% of the total body mass (van Waerebeek and Read 1994), but
almost all of the cetacean species examined have testes residuals above the regression line for
all mammals (Figure 4.2).
The unique capacity among cetaceans to develop and support such large testes is an
interesting evolutionary consideration. Most mammals have scrotal testes, ostensibly an
80

adaptation to maintain the testes at a temperature conducive to spermatogenesis (Moore
1926; Wislocki 1933; Waites 2012). Several other hypotheses for the origin of scrotal testes
have been proposed, including the elimination of problems associated with intra-abdominal
pressure that internal testes encounter (Chance 1996; Kleisner et al. 2010) Scrotal testes may
face a size limit, however, due to the potential for interference with locomotion. Cetacean
testes, on the other hand, are cryptic, lying within the abdominal cavity (Meek 1918; Slijper
1966). This positioning facilitates a streamlined body line for hydrodynamic locomotion, but
also exposes the testes to high core body temperatures, which are potentially detrimental to
spermatogenesis (Waites 2012).
Cetaceans have evolved a counter-current heat exchange system wherein arterial blood
supplying the intra-abdominal testes is cooled by close contact with veins that drain the dorsal
fin and flukes (Rommel et al. 1992). Those veins pass very close to the surface of the dorsal fin
and flukes and are exposed to the ambient cold water, providing a mechanism to keep the
testes at a temperature optimal for sperm production. The capacity for cetaceans to evolve
relative testes so much larger than other mammals may be a result of the efficient cooling
mechanism. Alternatively, larger testes might be metabolically cheaper to maintain in a
buoyant, aquatically adapted body.
Although the correlation between maximum body mass and relative testes mass was
significantly higher in “all mammals” than it was in cetaceans (r = 0.93 and 0.75 respectively; z =
3.81 with p = 0.0001), the cetacean model still has important explanatory power. The slopes of
the lines described were not significantly different (t = 1.908; p = 0.058, DF = 178), but the
81

intercept for the cetacean equation was significantly higher than for “all mammals” (t = 9.108; p
< 0.0001, DF = 178). Thus, there are differences in the magnitude of testes size increase
between the two models, but not the rate of testes size increase. This disparity is likely driven
by the intrinsic propensity for cetaceans to have testes much larger than expected for their
body sizes, coupled with the extreme difference in body sizes of the species included in the two
different analyses. Body mass ranged from a 5 gram shrew to a 50 ton baleen whale in the all
mammal analysis (Kenagy and Trombulak 1986), while even the smallest porpoise used in the
cetacean analysis (the vaquita, at 46.7 kg) can be considered a moderately large mammal.
Since information available on reproductive behaviors and mating strategies is limited
or even non-existent for most cetacean species, developing a model that uses relative testes
mass as an indicator of mating ecology will allow better predictions for species from which little
is known. A better understanding of mating strategies can, for example, influence species
management and conservation decisions. Highly polygynous species, where only a few males
contribute to the gene pool, may take longer to recover from a population bottleneck caused
by commercial whaling.
A linear model can also prove useful in teasing apart the variability of male mating
strategies within a species. For example, there are two geographic populations of the spinner
dolphin, Stenella longirostris, each have differing testes mass averages and patterns of sexual
dimorphism (Perrin and Mesnick 2003). Eastern spinner dolphins show distinct sexual
dimorphism with males having forward-canted dorsal fins, while sexes in the western form is
essentially monomorphic. The eastern morph also has lower average and maximum testes size
82

compared to the western form. Accordingly, the two forms of spinner dolphin likely exhibit
divergent mating strategies and therefore require different conservation schemes (Perrin and
Mesnick 2003).
In summary, relative testes size varies widely within Cetacea and there is a strong
positive correlation between body mass and testes mass. In addition, many species have testes
much larger than predicted by their body size, while others have testes smaller than expected
based on their body size. Cetaceans with large relative testes exhibit other features consistent
with promiscuous mating systems, such as mating in large groups and simultaneous
copulations. On the other hand, species with inferred pre-copulatory sexual selection, for
example species where males exhibit weapons used in intra-sexual aggression, have smaller
than predicted testes. These patterns suggest variation in sperm competition among cetaceans,
which is consistent with other groups with internal fertilization, including other marine and
terrestrial mammals.
Having established that relative testes mass is a good predictor of the intensity of sperm
competition in cetaceans, relative size of testes can be used to infer mating ecology. Species
with testes smaller than expected for their body mass are expected to be monogamous or
strongly polygynous (e.g., a single male controlling a large number of females). Conversely,
species with testes larger than predicted for their body mass are expected to be in a
promiscuous mating system. Information about mating ecology, as inferred from relative testes
size, can be used to explain variation in other structures used for reproduction. For example,
relative penis length in baleen whales has been shown to correlate with relative testes size
83

(Brownell and Ralls 1986). The relationships of testes mass, penis length, and pelvic bone size
and shape in cetaceans will be explored in the following chapter.

84

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91

Figure 4.1. Relative testes mass among 133 mammalian species. Modified from Kenagy and
Trombulak (1986), each coordinate represents one of 133 different species of mammal. The
equation for the regression line is Y=0.035X
0.72
; r
2
=0.86.
92

Figure 4.2. Relative testes mass among 49 species in Cetacea. The log of maximum body mass
was regressed against the log of maximum testes mass for each of the 49 cetacean species for
which data was available, and superimposed on the same data from Figure 4.1. Numbers
represent the cetacean species as identified below; gray points represent “all mammals”
species from Figure 4.1. Solid blue line is the best fit regression for the cetacean data
(Y=0.2207X
0.5722
; r
2
=0.58, p=<0.001); dashed line is the regression for 133 species of mammals
93

(Y=0.035X
0.72
) analyzed in Kenagy and Trombulak (1986). Residuals are taken as a measure of
relative testes sizes and are therefore an estimate of the strength of sperm competition. Large
positive residuals infer strong sperm competition; large negative residuals infer lack of sperm
competition. 1. Balaena mysticetus (bowhead); 2. Balaenoptera acutorostrata (minke whale);
3. B. borealis; 4. B. edeni; 5. B. musculus (blue whale); 6. B. physalus (fin whale); 7. Berardius
bairdii (Baird’s beaked whale); 8. Caperea marginata (pygmy right whale); 9. Cephalorhynchus
commersonii (Commerson’s dolphin); 10. C. hectori (Hector’s dolphin); 11. Delphinus capensis
(long-beaked common dolphin); 12. D. delphis (short-beaked common dolphin); 13. Eschrichtius
robustus (gray whale); 14. Eubalaena australis (southern right whale); 15. E. glacialis (northern
right whale); 16. Feresa attenuata (pygmy killer whale); 17. Globicephala macrorhynchus (pilot
whale); 18. Globicephala melas (pilot whale); 19. Grampus griseus (Risso’s dolphin); 20.
Hyperoodon ampullatus (bottlenose whale); 21. Inia geoffrensis (boto); 22. Kogia breviceps
(pygmy sperm whale); 23. Kogia sima (dwarf sperm whale); 24. Lagenorhynchus obscurus
(dusky dolphin); 25. L. acutus (Atlantic white-sided dolphin); 26. L. obliquidens (Pacific white-
sided dolphin); 27. Lissodelphis borealis (Northern right whale dolphin); 28. Megaptera
novaeangliae (humpback whale); 29. Mesoplodon carlhubbsi (Hubb’s beaked whale); 30.
Monodon monoceros (narwhal); 31. Neophocaena phocaenoides (finless porpoise); 32. Orcinus
orca (killer whale); 33. Peponocephala electra (melon-headed whale); 34. Phocoena phocoena
(harbor porpoise); 35. Phocoenoides dalli (Dall’s porpoise); 36. Phocoena sinus (vaquita): 37.
Phocoena spinipinnis (Burmeister's porpoise); 38. Physeter macrocephalus (sperm whale); 39.
Pontoporia blainvillei (franciscana); 40. Pseudorca crassidens (false killer whale); 41. Sotalia
fluviatilis (tucuxi); 42. Stenella attenuata (pantropical spotted dolphin); 43. Stenella
94

coeruleoalba (striped dolphin); 44. Stenella frontalis (Atlantic spotted dolphin); 45. Stenella
longirostris (spinner dolphin, whitebelly morph); 46. Steno bredanensis (rough-toothed
dolphin); 47. Tursiops aduncus (Indo-Pacific bottlenose dolphin); 48. Tursiops truncatus
(bottlenose dolphin); 49. Ziphius cavirostris (Cuvier’s beaked whale).

95

Figure 4.3 Tradeoff between investment in weapons and investment in testes. Numbers
represent the same species as in Figure 4.2 Species that invest in weapons or other traits useful
in pre-copulatory battles have a concomitantly decreased investment in testes size, shown here
as a negative residual for log testes mass vs. log body mass. Species with males having battle
teeth or tusks all have negative residuals. These include, in red: Mo_mo=Monodon monoceros
96

(narwhal), Me_ca=Mesoplodon carlhubbsi (Hubb’s beaked whale), Zi_ca=Ziphius cavirostris
(Cuvier’s beaked whale), Hy_am=Hyperoodon ampullatus (bottlenose whale), and
Be_ba=Berardius bairdii (Baird’s beaked whale). Species exhibiting sexual size dimorphism (in
green) also have negative testes residuals: Ph_da=Phocoenoides dalli (Dall’s porpoise) and
Ph_ma=Physeter macrocephalus (sperm whale). The species highlighted in purple is
Me_no=Megaptera novaeangliae (humpback whale). Humpback males use complex songs to
attract receptive females and engage in aggressive behaviors to establish dominance among
rival males.
97

Table 4.1. Mating systems
Mating System Intersexual interaction
Monogamy One male, one female
Polygamy Multiple mates
Polygyny One male, two or more females
Polyandry Two or more males, one female
Promiscuous Any male mates with any female

98

Table 4.2. Life history data for Cetacea
Species
Maximum
length
(cm)
Maximum
mass
(g)

Log
maximum
mass
Maximum
testes
mass
Log
maximum
testes mass
Testes
residuals
References
Balaena mysticetus 1800 90000000 7.954243 163000 5.212188 0.440546 Burns et al. 1993
Balaenoptera
acutorostrata
880 9200000 6.963788 8800 3.944483 -0.255507 Tomlin 1967
Balaenoptera borealis 1520 22000000 7.342423 16400 4.214844 -0.203679 Perry et al. 1999
Balaenoptera edeni 1500 40000000 7.602060 20000 4.301030 -0.267346 Tomlin 1967
Balaenoptera musculus 2700 150000000 8.176091 70000 4.845098 -0.054586 Tomlin 1967
Balaenoptera physalus 2400 90000000 7.954243 58300 4.765669 -0.005973 Panfilov 1978
Berardius bairdii 1280 12800000 7.107210 17600 4.245513 -0.037255 Mead 1984; Rice 1963;
Balcomb 1989
Caperea marginata 645 2850000 6.454845 1872 3.272306 -0.633942 Baker 1985
Cephalorhynchus
commersonii
174 86000 4.934498 930 2.968483 -0.060280 Goodall 1994
Cephalorhynchus hectori 138 53000 4.724276 1210 3.082785 0.175355 Slooten and Dawson 1994
Delphinus capensis

235 235000 5.371068 6414 3.807129 0.513069 unpublished data, LACM
Delphinus delphis 260 200000 5.301030 8170 3.912222 0.671911 Murphy et al. 2005
Eschrichtius robustus 1500 45000000 7.653213 67500 4.829304 0.231405 Tomlin 1967
Eubalaena australis 1700 90000000 7.954243 972000 5.987666 1.216025 Best et al. 2001; Omura et
al. 1969
Eubalaena glacialis 1700 90000000 7.954243 972000 5.987666 1.216025 Best et al. 2001; Omura et
al. 1969
Feresa attenuata 264 225000 5.352183 754 2.877371 -0.392463 Harrison et al. 1972
99

Species
Maximum
length
(cm)
Maximum
mass
(g)

Log
maximum
mass
Maximum
testes
mass
Log
maximum
testes mass
Testes
residuals
References
Globicephala
macrorhynchus
700 3600000 6.556303 7000 3.845098 -0.119707 Kasuya and Marsh 1984
Globicephala melas 670 2320000 6.365488 12300 4.089905 0.235231 Desportes et al. 1993;
Bernard and Reilly 1999
Grampus griseus 383 500000 5.698970 10600 4.025306 0.555320 Jefferson et al. 2008;
Perrin and Reilly 1984
Hyperoodon ampullatus 980 7000000 6.845098 2600 3.414973 -0.716513 Benjaminsen and
Christensen 1979; Mead
1984; Mead 1989
Inia geoffrensis 255 207000 5.315970 1600 3.204120 -0.044814 Best and da Silva 1984
Kogia breviceps 425 417000 5.620136 10000 4.000000 0.575514 Bloodworth and Odell
2008; Caldwell et al.
1971; Ruiz et al. 1993
Kogia sima 270 280000 5.447158 4850 3.685742 0.348142 Ross 1979; unpublished
data, LACM
Lagenorhynchus obscurus 211 85000 4.929419 9730 3.988113 0.962281 van Waerebeek and Read
1994; Brownell and
Cipriano 1999
Lagenorhynchus acutus 280 235000 5.371068 740 2.869232 -0.411502 Reeves et al. 1999

Lagenorhynchus
obliquidens
250 200000 5.301030 1107 3.044148 -0.196163 Harrison et al. 1972
Lissodelphis borealis 307 115000 5.060698 1410 3.149219 0.047619 Harrison et al. 1972
Megaptera novaeangliae 1700 41000000 7.612784 4000 3.602060 -0.972505 Nishiwaki 1959; Brownell
and Ralls 1986
Mesoplodon carlhubbsi 532 1500000 6.176091 510 2.707570 -1.037792 Mead 1984; Mead et al.
1982
100

Species
Maximum
length
(cm)
Maximum
mass
(g)

Log
maximum
mass
Maximum
testes
mass
Log
maximum
testes mass
Testes
residuals
References
Monodon monoceros 465 1577000 6.197832 1778 3.249932 -0.507978 Gerson and Hickie 1985;
Hay and Mansfield 1989
Neophocaena
phocaenoides
200 55000 4.740363 863 2.936011 0.019295 Kasuya 1999
Orcinus orca 975 10488000 7.020693 23100 4.363612 0.130779 Dahlheim and Heyning
1999; Heyning and
Dahlheim 1988
Peponocephala electra 278 275000 5.439333 4500 3.653213 0.333079 Perryman et al. 1994
Phocoena phocoena 168 61000 4.785330 3515 3.545925 0.603257 Read 1999; Harrison 1969
Phocoenoides dalli 196 170000 5.230449 560 2.748188 -0.451386 Houck and Jefferson
1999; Ferrero and Walker
1999
Phocoena sinus 144 46700 4.669 1837.2 3.264156 0.388446 Vidal 1995; Hohn et al.
1996
Phocoena spinipinnis 183 79000 4.897627 680 2.832509 -0.174973 Brownell and Clapham
1999; Reyes and van
Waerebeek 1995
Physeter macrocephalus 1800 57000000 7.755875 12000 4.079181 -0.577970 Rice 1989
Pontoporia blainvillei 160 50000 4.698970 10.8 1.033424 -1.859401 Panebianco et al. 2012;
Danilewicz et al. 2004
Pseudorca crassidens 600 2000000 6.301030 14800 4.170262 0.352790 Perrin and Reilly 1984
Sotalia fluviatilis 182 53000 4.724276 2110 3.324282 0.416852 Best and da Silva 1984
Stenella attenuata 257 119000 5.075547 2896 3.461799 0.351628 Hohn et al.1985: Perrin
and Hohn 1994
Stenella coeruleoalba 256 156000 5.193125 500 2.698970 -0.479062 Perrin et al. 1994b;
Miyazaki 1984
Stenella frontalis 230 140000 5.146128 1210 3.082785 -0.068122 Perrin et al. 1994a
Stenella longirostris 235 82000 4.913814 2708 3.432649 0.415824 Perrin and Gilpatrick
1994
101

Species
Maximum
length
(cm)
Maximum
mass
(g)

Log
maximum
mass
Maximum
testes
mass
Log
maximum
testes mass
Testes
residuals
References
Steno bredanensis 265 155000 5.190332 3000 3.477121 0.300701 Miyazaki and Perrin 1994
Tursiops aduncus 270 230000 5.361728 2050 3.311754 0.036411 Kemper et al. 2014
Tursiops truncatus 381 650000 5.812913 1966 3.293584 -0.242166 Perrin and Reilly 1984
Ziphius cavirostris 700 3000000 6.477121 4200 3.623249 -0.295856 Mead 1984; Omura et al.
1955; Heyning 1989

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Table 4.3. Results from regression analyses

Model r Intercept Slope
Standard
Error
slope

Residual
Sum of
Squares
Standard
Deviation
x

n
Cetacea 0.75213 0.221 0.572 0.07313 15.208 1.122782 49
All Mammals 0.92626 -1.456 0.72 0.02549 24.977 1.154177 133

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Chapter 5 – Cetacean pelvic bones respond to sexual selection
INTRODUCTION
The absence of external hindlimbs is among the most salient features separating extant
cetaceans from other mammals. Internal remnants of the pelvic girdle and hindlimbs, however,
are found in varying degrees in living whales and dolphins, embedded within the musculature
of the ventral body wall and dissociated from the vertebral column (Abel 1907; Lönnberg 1910;
Slijper 1979). Paired rod-like bones representing the vestiges of the pelvic girdle are found in all
living cetacean species except in the genus Kogia, which possesses ligamentous sheaths in place
of ossified bones (Benham 1901b, 1902; Schulte and Smith 1918). Among the baleen whales, or
mysticetes, ossified or cartilaginous vestiges of femora and tibiae commonly occur in addition
to pelvic bones (Eschricht and Rheinhart 1866; Struthers 1881; Howell 1930; Omura 1980).
Although rare, atavistic manifestations of hindlimbs have been observed in many species,
including humpback whales (Andrews 1921), sperm whales (Ogawa and Kamiya 1957; Nemoto
1963; Berzin 1972; Yablokov et al. 1974; Deimer 1977) and bottlenose dolphins (Ohsumi 2008).
As in snakes and other limbless tetrapods, the loss of external hindlimbs in cetaceans is
polygenic, involving genes with pleiotropic effects (Lande 1978; Bejder and Hall 2002). Genes
involved with limb development also control the ontogeny of other structures, including the
genitalia (Rosa‐Molinar and Burke 2002); therefore, it’s not unexpected that some elements of
the hindlimbs haven’t entirely disappeared in cetaceans. In fact, during early development,
cetacean embryos form hindlimb buds that regress as gestation progresses (Sedmera et al.
1997; Richardson and Oelschläger 2002; Thewissen and Heyning 2007; Fig. 5.1). These buds
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apparently persist longer in mysticetes such as the humpback whale, Megaptera novaeangliae,
than in odontocetes, which may explain why baleen whales often retain elements of the
hindlimb skeleton whereas odontocetes do not (Bejder and Hall 2002).
The origin of cetaceans and their transition from land to an aquatic existence has been
intensely researched by evolutionary biologists (reviewed, for example, in Uhen 2010), but few
studies have focused on the nature of the enigmatic pelvic bones in living whales and dolphins.
Even as the terrestrial ancestry of cetaceans has been elucidated with fossil discoveries of
quadrupedal “walking whales” (Gingerich and Russell 1981; Gingerich et al. 2001; Thewissen et
al. 2001; Gingerich 2003), and even as the loss of external appendages and dramatic reduction
of the pelvic girdle has been explained in terms of improved hydrodynamics (Fish 1992, 1993;
Fish et al. 2008), the significance of why small paired pelvic bones have persisted despite 40
million years of evolution with no role in supporting any hindlimbs has remained largely
unresolved. Indeed, textbooks commonly refer to the cetacean pelvic bones as vestigial
structures (Feldhamer et al. 2003) or even as “useless vestiges” (Curtis and Barnes 1989),
which has led to the common perception that cetacean pelvic bones are without function and
on an evolutionary trajectory of being lost.
Vestigial structures, although commonly interpreted as non-functional and therefore
non-adaptive characters, may nevertheless be retained for functions other than the one
traditionally assigned to the character, or even retained for secondary functions (Hall 2003,
2007). The latter appears to be the case for pelvic bones in cetaceans. It has long been
recognized that pelvic bones in cetaceans, as in all tetrapods, are the points of origin for the
ischiocavernosus muscles associated with and inserting upon the genitalia (Struthers 1881;
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Daudt 1898; Hepburn and Waterston 1904; Meek 1918; Ommanney 1932; Slijper 1966; de
Smet 1974; Rommel et al. 2007). While vestigial in the sense of no longer supporting external
hindlimbs, cetacean pelvic bones retain the function of anchoring the genitalia and associated
muscles, providing an explaining for the retention of these structures in modern taxa.
Moreover, since pelvic bones in modern cetaceans are not constrained by hindlimb attachment
and locomotion, they are potentially free to evolve in association with reproductive parameters
such as mating ecology.
Among cetaceans, as in all sexually reproducing taxa, mating strategies are diverse,
complex and highly variable (Mesnick and Ralls 2009). Males and females of the same species
often adopt differing strategies to ensure reproductive success. With plentiful gametes, the
typical strategy among males is to mate with as many females as possible. Females, on the
other hand, with limited ova, tend to maximize their reproductive success by mating with high
quality males, thus producing high quality offspring. These divergent strategies lead to a true
“battle of the sexes” and in turn engender divergent reproductive success among the
individuals comprising that species (Bateman 1948).
Sexual selection arises from differences in reproductive success caused by competition
for mates (Darwin 1871; Andersson 1994). The concept of sexual selection has been used to
explain how species evolve characters that help them increase their reproductive success, or
fitness, while those very same characters have the potential to be detrimental to an individual’s
short-term survival. For example, male songbirds typically exhibit colorful feathers and distinct
songs or calls to attract female mates, but those same feathers and songs may also attract
potential predators. Sexual selection has also been used to explain the dramatic variation
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observed in characters involved, directly or indirectly, in sexual reproduction. Structures
associated with reproduction are the most rapidly evolving of structures. Male genitalia, for
example, have been shown to evolve more rapidly than any other morphological feature
(Eberhard 1985).
Within Cetacea, variation in structures associated with reproduction can be attributed
to sexual selection. The cetacean penis is highly maneuverable and can, for example, be
deployed to overcome female mating resistance behavior (Mate et al. 2005). Moreover, in
North Atlantic right whales (Eubalaena glacialis), the species with the longest known penis,
multiple males have been observed attempting to simultaneously copulate with one female,
and males in this species are known to have enormous testes relative to their overall body size
(Mate et al. 2005). Testes mass, penis length, and simultaneous copulation behavior in right
whales are consistent with a strategy of intense post-copulatory competition. Species with
different mating strategies are expected to present variability in morphology of structures
associated with reproduction. Across ten species of baleen whales examined by Brownell and
Ralls (1986), the relative penis length was significantly correlated with relative testes mass.
Relative testes mass is a well-established, reliable proxy for the intensity of post-copulatory
sexual selection (Harcourt et al. 1981; Kenagy and Trombulak 1986; Møller 1989; Gage 1994;
Stockley et al. 1997; Hosken 1998; Hosken and Ward 2001; Ramm et al. 2005; Firman and
Simmons 2008). The result of Brownell and Ralls (1986) therefore suggests a relationship
between mating strategy and penis length in baleen whales, but their analysis unfortunately did
not account for potential biases stemming from the phylogenetic affinities of the specimens
they examined. Modern baleen whales are so closely related that half of the living species are
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congeneric, in the genus Balaenoptera. In addition to differences in penis length among species,
considerable variation has been noted in the size and shape of cetacean pelvic bones, both
within and between species (Struthers 1881; Hosokawa 1951; van Deinse 1954; Heyerdahl
1973; van Bree 1973; Deimer 1974; Perrin 1975; Deimer 1977; Andersen et al. 1992; McLellan
et al. 2002). In spite of this, the possible correlation between pelvic bone morphology and penis
length in cetaceans has never been examined.
Although the selective forces that determine mating ecology are complex (Clutton-Brock
2007), there are at least two main categories of sexual selection: intrasexual competition and
intersexual competition, or mate choice. Intrasexual competition may take the form of male-
male fighting, which is frequently accompanied by sexual dimorphism. The presence of
weapons, such as teeth or tusks, in males but not females, is usually interpreted as evidence of
male to male combat. Within Cetacea, this is a common strategy among beaked whales
(McCann 1974) and narwhals (Silverman and Dunbar 1980). Rake marks, or scarring patterns on
the body of male toothed whales that match the shape and positions of teeth of conspecifics,
provide consistent evidence of this strategy (Norris 1967), although Connor et al. (2000) caution
that reliance on the presence of external scars probably leads to an underestimate of the
species using this stratagem. The extremely dense, or pachyosteosclerotic, bone that replaces
the typically cartilaginous meso-rostral canal in some beaked whales provides additional
evidence of male-male fighting among this group (Heyning 1984). The rostrum of the beaked
whale Mesoplodon densirostris, for example, has the densest bone found in any mammal (De
Buffrenil and Casinos 1995). Intrasexual competition, manifested as combat between males, is
common in species that exhibit polygyny (Andersson 1994).
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Another form of intrasexual conflict is sperm competition, wherein the struggle
between individual males takes place on the gamete level (Parker 1970; Parker 1984). Among
promiscuous species, selection should favor those males capable of producing large volumes of
sperm by enabling them to flush out the ejaculate of competing males that previously mated
with a particular female, or simply by overwhelming the numbers of a competitor’s sperm
present in the target female’s reproductive tract (Parker 1990). To the extent that the capacity
to produce large volumes of sperm is reflected in testis size, size of testes may correlate with
mating system. Specifically, for a given body size, testis size should correlate with degree of
female promiscuity in that species (Harcourt et al. 1981; Kenagy and Trombulak 1986; Møller
1989, 1991; Gage 1994; Hosken 1998; Hosken and Ward 2001; Eberhard 2009). This is seen
among rodents, for example, as varying levels of sperm competition account for variation in the
relative size of the testes (Figure 5.2; Ramm et al. 2005; Firman and Simmons 2008). Most
mammals, in fact, appear to be predisposed to polygyny and sperm competition (Clutton-Brock
1989). It is therefore not surprising that for cetaceans, as in many other mammalian taxa,
sperm competition is a pervasive evolutionary force, shaping their reproductive anatomy,
physiology and behavior (Connor et al. 2000).
In contrast to intrasexual conflict, intersexual competition typically takes the form of
female choice, wherein females may select male partners based on courtship displays,
successful combat bouts, or even subtle or cryptic cues (Eberhard 1996). Male humpback
whales (Megaptera novaeangliae) are known, for example, for long and elaborate vocalizations
during breeding season, a behavior associated with attracting receptive females (Tyack 1981).
Length and complexity of a male’s song may give an indication of his fitness to potential mates.
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Furthermore, the dynamic nature of the vocalizations led Tyack (1981) to suggest that changes
in the song might be driven by female choice. The true function of the humpback song remains
unresolved, however, as male humpback vocalizations may alternatively be explained as a
behavior used to establish dominance hierarchies within male herds (Darling and Bérubé 2001).
Similarly, “gunshot” vocalizations observed in male North Atlantic right whales (Eubalaena
glacialis) may function as an advertisement signal to attract females, as an agonistic signal
directed toward other males, or some combination of the two (Parks and Tyack 2005). The
songs of blue whales (Balaenoptera musculus) and fin whales (B. physalus), meanwhile, are less
complex than those of humpbacks, but both species are solitary rovers in which only males
vocalize, suggesting that vocalizations, at least in those two species, are used to attract mates
(Clark 1990).
Female choice may also take place after copulation at the gamete level; a process
known as cryptic female choice, wherein females manipulate the paternity of their offspring by
preferentially selecting which sperm fertilize their ova (Eberhard 1996; Birkhead 2000;
Eberhard 2000). Cryptic female choice has been associated with many taxa, including salmonids
(Young et al. 2013); birds (Calsbeek and Sinervo 2003); and insects and arachnids (Eberhard
1994; Ward 2000; Welke and Schneider 2009). Indeed, cryptic female choice is widespread and
is recognized as an important component of sexual selection (Eberhard 1996). Establishing the
existence of cryptic female choice in marine mammals, however, remains elusive since
laboratory experimentation is unfeasible. One provocative indication of its importance in
cetaceans is the complex morphology described in the female reproductive tracts of many
different species of whales and dolphins. Elaborate folds of muscular tissue forming canals and
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blind sacs in the upper parts of the vagina have been described in Balaenoptera physalus
(Daudt 1898; Ommanney 1932), Phocoena phocoena (Daudt 1898; Meek 1918), and
Globicephala sp. (Murie 1873; Harrison 1949). It is tempting to propose that the function of the
vaginal folds and pockets in these cetaceans is for sperm storage and possibly for directing
preferred sperm to the cervix via muscular contraction. Alternatively, the complex structure
may just make insemination difficult, another form of female choice.
Under the sexual selection hypothesis, selection on male genitalia is caused by
processes that generate variation in post-copulatory paternity success among males (Arnqvist
1998; Lemaître et al. 2012). These processes include sperm competition, cryptic female choice,
and the intersexual conflict that develops over the control of fertilization (i.e., an evolutionary
arms race) (Arnqvist 1998; Arnqvist and Rowe 2005). A fundamental prediction of this
hypothesis concerns the rate of genital evolution as it relates to mating system (Eberhard
1985). In species where females normally mate with only one male (i.e., monandry), there is
expected to be little variation in male mating success and post-copulatory sexual selection on
genitalia will therefore be negligible or absent. In promiscuous species, however, variability in
male mating success will lead to intraspecific variation in genital morphology (Arnqvist 1998;
Hosken and Stockley 2004; Ramm 2007).
Against this background, the predictions of the post-mating sexual selection hypothesis
as it relates to the observed variation in cetacean pelvic bone morphology were tested.
Specifically, mating ecology, as inferred from relative testes size, is expected to influence the
degree of variation in the shape and size of cetacean pelvic bones. As anchors for the
ischiocavernosus muscles, pelvic bones are internal extensions of the genitalia, providing
111

important structural support for the genitalia and the muscles that control them. It is expected
that cetacean species inferred to be promiscuous based on relative testes mass will
correspondingly have relatively longer penises and will therefore also have relatively larger and
more robust pelvic bones to support the larger penises. Conversely, cetacean species inferred
to be less promiscuous based on relative testes mass will tend to have smaller relative penises
and, concomitantly, relatively smaller pelvic bones. In addition, it is hypothesized that more
promiscuous species may benefit from having pelvic bones with a more complex morphology.
Variable mating success among males may result, for example, from variations present on the
pelvic bone surface that impart idiosyncratic manipulation of the penis.

METHODS
Reanalysis of penis length in baleen whales
Brownell and Ralls (1986) found a significant correlation between testes mass and penis
length in 10 species of mysticete whales. However, closely related species tend to have similar
trait values because they share most of their evolutionary history. For the present study, data
presented in Table 2 of Brownell and Ralls (1986) were re-analyzed to account for the
phylogenetic relatedness of the living baleen whales. A generalized least squares (GLS)
approach provides a natural framework in which to represent features that arise from
phylogenetic affinities, while simultaneously estimating the variance parameter of trait
evolution (Pagel 1999). Using the GLS procedure in the R package NLME (Pinheiro et al. 2013)
and the corPagel procedure in the R package APE (Paradis et al. 2004), regressions were
112

performed within the molecular phylogenetic framework of McGowen et al. (2009) to derive (a)
the residual of penis length onto body mass and, (b) the residual of testes mass onto body
mass. A third regression analysis, performed within the same phylogenetic context, tested the
correlation of residual penis length with residual testes mass.

Specimens
The left and right pelvic bones from more than 250 specimens comprising 35 cetacean
species were obtained from museum collections. To account for ontogenetic variation, only
pelvic bones from individuals that could be identified as sexually mature were included in the
analyses. Sexual maturity was determined by comparing the recorded body length of the
specimen with published minimum body lengths for sexually mature individuals in those
species (Table 5.1). Specimens with total body lengths below the published minimum lengths,
as well as specimens of unknown length and unknown sex were excluded from analyses. After
eliminating non-adult specimens, a total of 133 cetacean specimens were included in the
analyses (Table 5.2), including 97 males from 24 species and 33 females from 14 species.
As a negative control, the left and right first vertebral ribs from the same individual
specimens were also obtained from museum collections. The first vertebral ribs have no
connection with genitalia and have no known role in reproduction, but are unique in their
morphology and easy to identify, making them useful as a control. Ribs from the large baleen
whales were too large for the equipment and were not included in the analyses. A total 87 male
specimens from 20 species included ribs, while 27 female specimens from 12 species included
113

ribs. To detect possible biases, the subset of specimens that included ribs in addition to pelvic
bones was separately subjected to the same statistical analyses as the larger group of samples.
Laser scanning
Bones were scanned using a NextEngine 2020i three-dimensional portable laser scanner
(NextEngine, Inc., Santa Monica, CA) controlled with ScanStudio HD v.1.3.0 software (Shape
Tools LLC, Santa Monica, CA) running on a Windows 7 laptop PC. Detailed scanner settings are
discussed in Chapter 2 and listed in Table 2.2. For each scanned bone, scan families were
merged and excess geometric data was removed using ScanStudio HD software or MeshLab
v.1.3.2 software (http://meshlab.sourceforge.net), producing mesh models comprising tens of
thousands of 3-dimensional coordinates representing digitized bones. Files were saved as text
files with each line in the file representing a single coordinate with x, y, and z values. Text files
were analyzed using geometric morphometric methods via a computational pipeline developed
uniquely for this project.

Landmark acquisition and geometric morphometrics
Geometric morphometric and computational analyses were performed using Python
(Rossum and Drake 2001) or performed in the R scientific computing environment (R Core
Development Team 2012). Pelvic bones in cetaceans vary in complexity depending on species
as well as age and sex, but a general feature they share is the absence of definable landmarks.
While the lack of fixed homologous landmarks limits the utility of traditional morphometric
114

methods, the introduction of sliding semi-landmark analysis provides a novel method of
objective quantification of shape divergence (Gunz et al. 2005; Mitteroecker and Gunz 2009;
Van Bocxlaer and Schultheiß 2010).
To establish the polarity (i.e., anterior vs. posterior ends) of each bone’s digital model,
each data file was opened in R v.2.15.3 using the DIGIT.FIXED routine in the GEOMORPH
package (Adams and Otárola-Castillo 2012). For pelvic bones, one xyz coordinate was chosen at
the anterior end of the pelvic bone mesh model. For mesh models of ribs, three different xyz
coordinates representing the ventral end, the “head” and the “tubercle” of each rib were
identified. Digitizing these “landmarks” ensured the correct anterior-posterior alignment of the
mesh models before the automated computational processes downstream.
The computational pipeline developed to transform and define the geometric
coordinates from each bone is described in Chapter 2. Briefly, three “fixed” landmarks were
assigned to each mesh model, as computed by the convex hull (De Berg et al. 2008). A total of
962 semi-landmarks were spread evenly over the surface of each mesh model (see Figures 2.5
for pelvic bones and 2.6 for ribs). A large number of semi-landmarks were chosen to fully
capture detailed morphological differences in the bones. Using these transformed semi-
landmarks, centroid size and pairwise shape divergence were quantified among all pelvic bones
and, in separate analyses, all ribs. Centroid size of each bone was calculated as the square root
of the sum of squared distances of the semi-landmarks from their centroid.

115

Size Analysis I: Phylogenetic Regression Analyses
To estimate variation in post-copulatory sexual selection among cetaceans, reproductive
data from 42 species was collected from the literature (Table 5.1 and references therein). The
common logarithm (log to base 10, or log10) of the maximum recorded testes mass for each
species was then regressed against the log10 of the maximum recorded body length for each
species. The resulting residuals provided a measure of relative testes mass, a well-established
proxy for degree of post-copulatory sexual selection (Stockley et al. 1997; Hosken 1998; Ramm
et al. 2005). The regression was performed using a generalized least squares framework via the
GLS procedure in the R package NMLE (Pinheiro et al. 2013). To account for phylogenetic
affinities among the taxa (Pagel 1999), the GLS procedure included a correlation structure
obtained using the corPagel procedure in the R package APE (Paradis et al. 2004). The cetacean
phylogeny used was obtained from McGowen et al. (2009). The resulting residuals were used as
a measure of relative testes mass.
Similarly, to convert absolute pelvic bone centroid sizes to a relative measurement (i.e.,
to account for the effect of body size on pelvic bone centroid size), the log10 of the average
pelvic bone centroid values for each species (Table 5.2) were regressed against the log10
maximum body length values for those same species (Table 5.1). Only specimens representing
sexually mature males were included, which limited the analysis to 23 species. As in the
regression analysis of testes mass to body length, the GLS procedure in the R package NLME
(Pinheiro et al. 2013) was performed using a phylogenetic correlation structure obtained from
the corPagel procedure in the R package APE (Paradis et al. 2004). The residuals obtained in this
116

phylogenetically controlled regression represent the relative pelvic bone centroid sizes for the
23 species.
To assess the relationship between relative pelvic bone centroid size and relative testes
mass, the phylogenetic residuals of centroid size were regressed against the phylogenetic
residuals of testes mass. As in the previous regression analyses, the GLS procedure in the R
package NLME (Pinheiro et al. 2013) was performed using a phylogenetic correlation structure
obtained from the corPagel procedure in the R package APE (Paradis et al. 2004). This
regression analysis was limited to the 23 species for which male sexually mature specimens
were available.

Size Analysis II: Correlated Trait Evolution
To account for potential biases associated with correlated trait evolution, a separate
analysis was performed wherein a customized phylogenetic model was created where log body
length, log size of testes, and log centroid size of left and right pelvic bones and left and right
ribs evolved as a correlated multivariate Brownian motion on a cetacean phylogeny (Figure 5.3)
adapted from McGowen et al. (2009) and based on 45 nuclear loci, transposons and
mitochondrial genomes. A Bayesian analysis was performed based on Revell and Collar (2009),
but modified to incorporate uncertainties due to intraspecific variation, missing data, and the
measurement of different variables at the species and individual levels. Despite the absence of
morphometric data, uncertainty in the phylogeny wasn’t expected to be a significant
confounding factor and phylogenetic uncertainty was therefore not accounted for in the
117

analyses. Derivations used for the Bayesian methods were developed in collaboration with Dr.
Peter Ralph. Detailed descriptions found in the Supplementary Materials for Dines et al.
(Submitted) and are only summarized here.
First, variables were defined as the logarithm values of the traits included in the model:
L = log (body length) (1)
T = log (testes size) (2)
P
R
= log (right pelvic bone centroid size) (3)
P
L
= log (left pelvic bone centroid size) (4)
R
R
= log (right rib centroid size) (5)
R
L
= log (left rib centroid size) (6)
To characterize trait variation between species, the model was based on the formula
Z A t X X
t O
 
t
where X
O
= (L
O
, T
O
, R
R
O
, R
L
O
, P
R
O
, P
L
O
) is the mean for the trait values of the
ancestor species, X
t
= (L
t
, T
t
, R
R
t
, R
L
t
, P
R
t
, P
L
t
) is the mean trait values of the descendant species,
A
t
is parameterized in the covariance matrix below, and Z represents increments of Gaussian
(random) evolution of a given trait along the length of a given tree branch.
118

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

















4
3
2
1
0
0
0
0
0
0
0
0
0
0
0 0
0 0 0
Z
Z
Z
Z
t
P
P
R
R
T
L
P
P
R
R
T
L
P P P
P P P
R R R
R R R
T T
L
L
R
L
R
L
t
R
t
L
t
R
t
t
t
  
  
  
  
 

(7)
To characterize trait variation within species and within individuals, a similar
parameterization was used but instead with the formula BW X X
S
 
I
where species mean
trait values were X
S
= (L
S
, T
S
, R
R
S
, R
L
S
, P
R
S
, P
L
S
) and the trait values of an individual were X
I
= (L
I
, T
I
,
R
R
I
, R
L
I
, P
R
I
, P
L
I
). In this case W represents independent standard Gaussians, and B is
parameterized as in the covariance matrix below:






































    










































5
4
3
2
1
0 0
0 0
0 0
0 0
0 0 0 0
W
W
W
W
W
t
P
P
R
R
T
L
P
P
R
R
T
L
P P P
P P P
R R R
R R R
L
L
S
R
S
L
S
R
S
S
S
L
I
R
I
L
I
R
I
I
I
  
  
  
  

(8)
The row in matrix B corresponding to testes size is omitted because testes size was not
available for individual specimens. Maximum known testes mass was gathered from the
literature and used only for interspecies comparisons.
To estimate the proportion of changes in pelvic bone size that are due to shifts in mating
ecology relative to other causes, such as random drift or changes in species mean body length,
the following equation is used:
119

P P P
P
  

 
(9)
Similarly, the proportion of changes in rib size due to mating ecology relative to other causes is
computed by:
R R R
R
  

 
(10)

To ensure the results were not affected by patterns of missing data, a standard random-
walk Markov chain Monte Carlo (MCMC) sampler was implemented. The MCMC package for R
(Geyer and Johnson 2013) was used to estimate the posterior distribution of the above
parameters on three subsets of bone data: (a) all bones from all adult male cetaceans, (b) all
bones from all adult female cetaceans, and (c) all bones from adult male cetaceans for which
data from both pelvic bones and ribs was available. Ribs for the large baleen whales were too
large to be scanned, so were absent from the data. The subset (c) was therefore analyzed
separately to detect any misleading results from missing rib data in the analysis of (a). The
MCMC sampler was run for a total of 500,000 iterations for each of the three different datasets.
In each case, the first 20,000 iterations were discarded as burn-in, at which point trace plots
showed that convergence had been reached.

Shape Analyses
To assess shape variation, pairwise shape divergence within and between species was
quantified with the GPAGEN routine in the R package GEOMORPH (Adams and Otárola-Castillo
120

2012), which uses a Generalized Procrustes framework based on algorithms previously
developed in geometric morphometrics (Rohlf and Slice 1990; Bookstein 1997; Zelditch et al.
2004; Mitteroecker and Gunz 2009). A Generalized Procrustes Analysis translates all specimens
to a common origin, scales them to a common centroid size of 1, then optimally rotates the set
of coordinates using a least-squares criterion until all the coordinates of corresponding
landmarks align as closely as possible (Bookstein 1991). The resulting aligned Procrustes
coordinates describe differences in shape while minimalizing the effects of object’s size and
orientation. Semi-landmarks were allowed to “slide” along their tangent directions on the
surface of the mesh during the Procrustes superimposition, optimizing their locations by
minimizing the Procrustes distance between the reference specimen and the target specimen.
The use of sliding semi-landmarks improves alignment of regions that are hypothesized to share
homology while still maintaining structural integrity (Bookstein 1996; Bookstein 1997; Gunz et
al. 2005; Mitteroecker and Gunz 2009). Prior to the alignment procedure, left-sided bones were
transformed into their mirror-images to match with their right-sided counterparts. The sum of
the distance between aligned, corresponding landmarks was taken as the shape distance, or
Generalized Procrustes Distance (GPD) which was used for subsequent multivariate analyses.

Sexual Dimorphism
To test for intersexual variation in both size and shape of both pelvic bones and ribs, a
nested ANOVA was performed on the resulting distance matrices using the ADONIS function of
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the VEGAN package (Oksanen et al. 2013) in R. For the hypothesis tests 10,000 replicate
permutations were specified.

Technical Replication
To assess the repeatability of the three-dimensional laser scanner and the novel
computational techniques developed for this study, 41 bones (21 pelvic bones and 20 ribs)
were randomly selected and subjected to multiple scans with each unique scan run through the
computational pipeline. One pelvic bone was scanned 11 times, each time removing the bone
from the scanning platform and putting it back in place in a different orientation, slightly
different position, or slightly different distance from the laser scanner. The remaining 20 pelvic
bones and 20 ribs were each scanned twice, each time removing the bone from the platform
and replacing it in a slightly different position. Scanning the same bones in different positions
and subjecting the scans to downstream analyses allowed for the assessment of the accuracy
and repeatability of the laser scanner.

RESULTS
Reanalysis of penis length in baleen whales
The regression model of Figure 5.4 confirms the significant correlation between penis
length and testes mass observed in Brownell and Ralls (1986), even when accounting for
phylogenetic affinity among these closely related baleen whale species. Baleen whales with
122

relatively large testes have relatively large penises, while baleen whiles with relatively small
testes have relatively small penises.

Size Analysis I: Phylogenetic Regression Analyses
Table 5.1 lists the maximum recorded testes mass and maximum body length for 42
species representing 4 of the 4 families of modern baleen whales and 7 of the 10 families of
modern toothed whales. Combined left and right testes mass ranged from 10 grams in the
franciscana, Pontoporia blainvillei, a dolphin species that likely exhibits serial monogamy
(Danilewicz et al. 2004; Panebianco et al. 2012), to nearly 1 metric ton for the North Atlantic
right whale, Eubalaena glacialis, a balaenid with strong post-copulatory sexual selection (Mate
et al. 2005). These two species represent the two extremes in the resulting regression (Fig. 5.5),
with respective residuals well below and well above the regression line.
For the 23 cetacean species for which sexually mature specimens were available, the
average pelvic bone centroid size for each species was calculated and then regressed onto
maximum body length for those species (Fig. 5.6). The resulting residuals were used as a
measurement of relative pelvic bone size. Species with notably small values for relative pelvic
bone size include the franciscana, P. blainvillei, and Cuvier’s beaked whale, Ziphius cavirostris.
Species with notably high relative pelvic bone size include the harbor porpoise, Phocoena
phocoena, the gray whale, Eschrichtius robustus, and the North Atlantic right whale, Eubalaena
glacialis.
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The regression model in Figure 5.7 estimates the relationship between residual pelvic
bone centroid size and residual testes mass in the 23 species for which sexually mature adult
specimens were available. Pelvic bone centroid size residuals were significantly positively
correlated with testes mass residuals (p=0.0012). In other words, there was a significant
correlation between relative pelvic bone size and relative testes mass. Species inferred to
exhibit strong post-copulatory competition, by virtue of their relatively large testes mass, also
possessed relatively large pelvic bones. Conversely, species with relatively small testes and
therefore inferred to express very low post-copulatory competition, had small pelvic bones
relative to their body size.

Size Analysis II: Correlated Trait Evolution
For the model run on all adult male specimens, the posterior means are given in Table
5.3. Using equation (9) and taking the posterior mean values for pelvic bone centroid
(calculated as 0.7/(0.47 + 0.07 + 0.07) = 0.11), 11 percent of the changes in pelvic bone size is
derivable from shifts in testes size after removing the effects of changes in body length. Using
trait-specific posterior mean values from the same table, it was calculated that another 0.11 is
due to pelvic-specific noise, and 0.77 is a result of changes in body length. Further, the
summary statistics of the estimated posterior distributions for the model parameters (Table
5.4; Fig. 5.9) showed that pelvic bone centroid size in all adult males was strongly correlated
with increased testes mass (correlation rho = 0.67; 95% credible interval: 0.25 – 0.90). Taking
the posterior mean values for rib centroid size, 0% of the change in rib size was explained by
124

shifts in testes mass (calculated using equation (12) as: 0.00/0.51 + 0.00 + 0.04). There was no
correlation between rib centroid size and testes mass (correlation rho = 0.07; 95% credible
interval: -0.51 – 0.62). Finally, there was no correlation between pelvic bone centroid size and
rib size (correlation rho = 0.05; 95% credible interval: -0.38 – 0.48).
For the model run on adult male specimens with complete sets of pelvic bones and ribs
available, the posterior means and quartiles are given in Table 5.5 and the marginal posterior
distributions are shown in Table 5.6 and Fig. 5.10. The correlation between pelvic bone centroid
size and testes mass remained strong (correlation rho = 0.58, credible interval: -0.04 – 0.92),
while there was still no correlation between rib size and testes mass (correlation rho = 0.06,
credible interval: -0.52 – 0.64). Again, there was no correlation between pelvic bone centroid
size and rib size (correlation rho = 0.04, credible interval: -0.57 – 0.50).
Adult female specimens also showed a positive correlation between pelvic bone
centroid size and changes in maximum testes mass recorded for conspecific males (correlation
rho = 0.78, credible interval: 0.30 – 0.99; Table 5.7, Table 5.8, Fig. 5.11). Among females there
was a very low correlation between rib centroid size and the maximum testes mass recorded
for conspecific males (correlation rho = 0.20, credible interval: -0.58 – 0.80) and a very low
correlation between pelvic bones centroid size and rib size (correlation rho = 0.16, credible
interval: -0.48 – 0.69).

125

Shape analyses
Pairwise contrasts of testes divergence and pelvic bone shape divergence as well as
testes divergence and rib shape divergence were compared among 18 species comprising nine
species pairs, or taxa considered to be sister taxa based on the phylogeny of McGowen et al.
(2009). Only specimens from sexually mature males for which both pelvic bones and ribs were
available were analyzed, resulting in a lower number of included species. The 9 taxonomic
couplets were: (1) Delphinus capensis vs. D. delphis; (2) Feresa attenuata vs. Pseudorca
crassidens; (3) Grampus griseus vs. Steno bredanensis; (4) Inia geoffrensis vs. Pontoporia
blainvillei; (5) Lagenorhynchus acutus vs. Ziphius cavirostris; (6) Lagenorhynchus obliquidens vs.
Lissodelphis borealis; (7) Phocoenoides dalli vs. Phocoena phocoena; (8) Stenella attenuata vs.
Stenella longirostris; and (9) Stenella coeruleoalba vs. Stenella frontalis. Among the nine
independent species pairs, pelvic bone shape divergence was positively correlated with testes
residual divergence (Fig. 5.8C; p=0.008, r=0.81), while rib shape divergence was not correlated
with testes residual divergence (Fig. 5.8D; p=0.72, r=0.14).

Sexual Dimorphism
After accounting for species differences, sexual dimorphism was detected in the size
and the shape of pelvic bones as well as ribs within species. In a distance-based ANOVA of
pairwise differences in pelvic bone centroid size, sex as a source of variation in the model had
an F-value of 37.40 and the null hypothesis was rejected (Table 5.9). Similarly, for pairwise
differences in centroid size of rib, sex as a source of variation had an F-value of 4.88 leading to
126

rejection of the null hypothesis (Table 5.10). Sex also explained some of the variation in the
shape of pelvic bones and the shape of ribs, with F-values of 11.18 and 4.93 respectively (Tables
5.11 and 5.12).

Technical Replication
As long as the specimen was placed within the optimal range of the scanner, bone
morphology was accurately captured irrespective of specimen positioning. Size differences of
the scan replicates, quantified as the median coefficient of variation (unbiased standard
deviation/mean) for centroid size, was 0.0094 for pelvic bones and 0.0090 for ribs. Similarly,
the median coefficient of variation for pelvic bone shape was 0.0194 and for rib shape was
0.0342. The shape differences calculated between scan replicates was less than 5% of the
average pairwise shape difference among all bones. Surface scanning using the three-
dimensional laser scanning, as well as the computational pipeline developed to quantify size
and shape variances in the bones, were highly repeatable.

DISCUSSION
The pelvic bones of modern cetaceans are unique in that they are no longer constrained
by having a primary role in locomotion. The pelvic girdle in the typical tetrapod is fused with the
vertebral column and bridges the axial and appendicular skeletal elements to support the
127

hindlimbs. This ancestral condition was also present in the terrestrial ancestors of modern
cetaceans. In contrast, the pelvic bones of modern cetaceans are reduced paired structures that
are dissociated from the axial skeleton and do not support external hindlimbs. They do,
however, retain the primitive function of anchoring the ischiocavernosus muscles that support
the genitalia. The ischiocavernosus muscles (erector penis in males; erector clitoridis in females)
originate on the ischium and insert into the sides and under surface of the crus penis of males
and the crus clitoridis of females (Gray 1901). With their primary function shifted to supporting
the reproductive anatomy, pelvic bones are potentially free to diverge along with mating
ecology and evolve under the influence of sexual selection.
A reanalysis of previous work by Brownell and Ralls (1986) confirmed that species of
baleen whales with intense post-copulatory sexual selection, as inferred by having large relative
testes, have evolved long penises relative to their body size. By extension, it seems reasonable
to hypothesize that the infrastructure supporting the penis in cetaceans, namely the paired
erector penis muscles and the paired pelvic bones, would be subject to the same evolutionary
processes that select for a longer penis. In fact, two species with the largest relative pelvic
bones, the North Atlantic right whale (Eubalaena glacialis) and the harbor porpoise (Phocoena
phocoena) (see Fig. 5.5), also have the largest relative penis lengths. The right whale has a penis
nearly 15% of its total body length, the largest relative penis length among baleen whales (Fig.
5.4; Omura et al. 1969; Brownell and Ralls 1986). The harbor porpoise, one of the smallest
cetaceans, can have testes weighing as much as 2.7 kg and comprising more than 6% of its total
body mass (Fontaine and Barrette 1997). That mass is nearly as high as the testes mass
recorded for a fin whale (Balaenoptera physalus), the second largest species of cetacean with a
128

total body mass 1,000 times that of a harbor porpoise (Kenagy and Trombulak 1986). Harbor
porpoises have a penis as long as 1/3 of their total body length (Keener et al. 2011). It has been
suggested that longer penises observed in species with strong post-copulatory sexual selection
allow males to insert gametes closer to the female’s cervix, possibly facilitating successful
fertilization before a competitor’s sperm reaches the egg.
Among the 23 species for which sexually mature specimens were available, pelvic bone
centroid size in male cetaceans was highly correlated with relative testes mass, even after
accounting for phylogenetic dependence among those species (Fig. 5.7). Reliable penis length
data is not available for many of those species, but as shown above, degree of post-copulatory
competition correlates positively with penis length and penis length is, in turn, linked to pelvic
bone size. Relative testes mass is a good predictor of post-copulatory competition, so species
with low post-mating competition would be expected to exhibit small pelvic bones relative to
body size. With a combined testes mass of 10 grams, the franciscana dolphin (Pontoporia
blainvillei), has testes that are very small relative to body size (Fig. 5.5). Although monogamy in
franciscana dolphins was dubious to Brownell (1989) and to Connor et al. (2000), recent
analyses indicate this species exhibits serial monogamy (Panebianco et al. 2012). Franciscana
dolphins would therefore not be expected to exhibit post-copulatory sexual selection, leading
to the prediction that franciscana dolphins would have relatively small pelvic bones. In fact, the
pelvic bone centroid size residual for franciscanas is the smallest among Cetacea (Fig. 5.7).
Similarly, beaked whales such as Mesoplodon carlhubbsi and Ziphius cavirostris have
smaller testes than would be expected for their body masses (Fig. 5.5). Beaked whales typically
129

exhibit sexual dimorphism, with males possessing tusk-like teeth while females entirely lack
erupted teeth (Heyning and Mead 1996). Moreover, the heads of beaked whale males have
scar patterns that match conspecific tooth morphology, providing evidence of male-male
aggression and pre-copulatory competition; features consistent with a polygynous mating
system. Highly polygynous species typically possess relatively small testes as there is very weak
post-copulatory sexual selection (Fitzpatrick et al. 2012). As would be predicted due to low
relative testes mass, beaked whales (represented in our sample of 23 species by Ziphius
cavirostris) have relatively small pelvic bones (Fig. 5.7).
Since body length, testes mass, pelvic bone size and rib size are expected to evolve in a
correlated manner, a separate phylogenetic model was developed to account for possible
correlation among the traits being examined and run within a Bayesian framework to account
for uncertainties in the data. As in the regression analysis, pelvic bone centroid size was
strongly correlated with relative testes mass (Fig. 5.8A). In contrast, ribs, used as a negative
control because they aren’t involved in reproduction, had no correlation with testes mass (Fig.
5.8B). Within this model, data were also analyzed in three distinct subsets: (a) all sexually
mature males, including specimens with one or more ribs and/or one of the pelvic bones
missing; (b) sexually mature males, but only specimens with both ribs and both pelvic bones
present; and (c) all sexually mature females.
Among all sexually mature males, pelvic bone centroid size was highly correlated with
relative testes mass, even after accounting for body length evolution (rho = 0.67). Rib centroid
size was not correlated with testes (rho = 0.07), nor with pelvic bone centroid size (rho = 0.05),
130

indicating a unique relationship between pelvic centroid size and post-copulatory mating
system (Tables 5.3 and 5.4; Fig. 5.9). Similar results were obtained using the smaller data set
that included mature males for which both ribs and both pelvic bones were available (Tables
5.5 and 5.6; Fig. 5.10). Interestingly, female specimens also showed a positive correlation
between pelvic bone centroid size and testes (rho = 0.78, Table 5.8). Although testes are
obviously absent from females, the positive relationship between pelvic bones in females and
testes changes in conspecific males might be attributed to genetic correlations during
ontogenetic development. The strong sexual dimorphism observed in pelvic bones, however,
suggests that selection may be acting on unique but unknown aspects of female pelvic bones.
The pelvic bones in females is the origin for the erector clitoridis muscles (a.k.a. the
ischiocavernosus muscles), suggesting that clitoral movements might play a role in female
choice. Although speculative given the limited data here, cryptic female choice has elsewhere
been shown to play a significant, although until recently largely undetected, role in mating
ecology (Eberhard 1996). Recognizing cryptic female choice is challenging because it is not
obvious which male traits the female is selecting. The considerable variation occurring in male
pelvic bones, however, is a suggestive indication of female choice.
Among the 9 independent species pairs for which both pelvic bones and ribs could be
analyzed, pelvic bone shape divergence was positively correlated with the inferred divergence
of mating ecology (p = 0.008, r= 0.81) (Fig 5.8C). Within a species pair, the species inferred to
exhibit more post-copulatory competition (the inference was made by differences in average
testes mass for those species) exhibited more divergence in pelvic bone shape. Rib shape
divergence, on the other hand, was not correlated with the inferred divergence of mating
131

ecology (p = 0.72, r= 0.14) (Fig 5.8D). More promiscuous species may benefit from having pelvic
bones with more complex morphology. Shape variability may, for example, lead to variation in
penis maneuverability, divergent stimulation of female mates, and variable mating success
among males. The finding of shape divergence being correlated with mating ecology is
consistent with the notion that male genitalia evolve faster than any other structure (Eberhard
1985), particularly in promiscuous species (Arnqvist 1998).
Both pelvic bones and ribs were sexually dimorphic in both size and shape, after
accounting for species differences (distance-based ANOVA, McArdle and Anderson 2001,
Tables 4.9 - 4.12). Sexual dimorphism in pelvic bone shape has been previously reported in
porpoises (van Bree 1973; Andersen et al. 1992; Tajima et al. 2004), dolphins (Perrin 1975),
sperm whales (van Deinse 1954; Berzin 1972; Deimer 1977), and baleen whales (Heyerdahl
1973). Sexual dimorphism was also shown in the pelvic bones of manatees (Krauss 1872;
Domning 1991; Fagone et al. 2000), an unrelated group of secondarily aquatic mammals with
morphologies similar to cetaceans that represent parallel evolution. The widespread intersexual
variability in cetacean pelvic bones suggests they function in unique aspects of male and female
reproductive ecology.
Another finding was that the pelvic bones showed more bilateral asymmetry (measured
by coefficient of variation) than did the ribs (residual variance in Tables 4.9 – 5.12). There are
many possible explanations to this pattern, including relaxed selection or selection for novelty
in pelvic bones, but another possibility is heterochronic processes during ontogenetic
development. Studies in sticklebacks (Shapiro et al. 2004) and manatees (Shapiro et al. 2006)
132

found directional bilateral asymmetry in secondarily reduced pelvic structures, apparently due
to differential timing in the expression of the Pitx1 gene on the left and right sides of the body.
Similarly, Pitx1 knockout mice showed greater reduction of pelvic structures on the right side of
the body compared to the left (Marcil et al. 2003). The Shh gene has been associated with
reduction of the hindlimbs in snakes (Cohn and Tickle 1999), and Shh, Hand2 and Fgf8 are
apparently involved in the reduction of the hindlimbs in whales (Thewissen et al. 2006). Pitx1
appears to be a major regulator of downstream genes in developing hindlimb buds as well as in
development of the pelvic girdle itself (Itou et al. 2012). The asymmetry detected in cetacean
pelvic bones suggests there has been parallel evolution in the control genes responsible for
pelvic reduction in these widely divergent vertebrate lineages.

CONCLUSIONS
There is much evidence that contradicts the widely held perception that cetacean pelvic
bones are vestigial structures that are functionally non-essential. The earliest fully aquatic
whales (e.g., Basilosaurus of the middle Eocene, ~47 million years ago) retained external
hindlimbs too small to be used in swimming, and clearly not capable of supporting weight on
land (Gingerich et al. 1990). Since that time, pelvic bones in cetaceans have maintained the
other role of the generalized mammal pelvis: anchoring and supporting the reproductive
organs. In this role, cetacean pelvic bones are acted upon by evolutionary processes such as
sexual selection. Cetacean species with large relative testes, an indication of strong sexual
selection, have large penises and large erector penis muscles to control them. They also have
133

evolved relatively large pelvic bones. Furthermore, shape divergence of pelvic bones is
positively correlated with mating ecology. In other words, sexual selection, acting on the pelvic
bones supporting the genitalia and associated muscles, favors large and novel-shaped pelvic
bones. This pattern is not observed in ribs, used as a control because they are not involved in
support and control of the genitals. The reproductive function of pelvic bones in cetaceans,
coupled with the inherent patterns in their structure reject the notion of cetacean pelvic bones
being “useless vestiges.” To the contrary, cetacean pelvic bones are a critical component of
their reproductive fitness.

134

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Figure 5.1. Limb buds in a series of developing embryos of the pantropical spotted dolphin,
Stenella attenuata. Embryos (not shown to scale) increase in age from left to right, showing the
gradual formation of forelimb and hindlimb buds followed by reduction and resorbing of the
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150

Figure 5.2. The relationship, after controlling for phylogeny, between relative testis size and
percentage of litters with multiple paternity in rodents (Ramm et al. 2005). Species with
multiple paternity litters are subject to sperm competition. There is a strong correlation
between relative size of testes and the degree of sperm competition.

151

Figure 5.3. Cetacean phylogeny. Phylogeny of the 40 species examined in this study, based
upon the molecular phylogeny of McGowen et al. (2009). The first column to the right of the
tree lists the residual testes mass for the species. High positive numbers infer a mating system
with intense post-copulatory selection; high negative numbers infer mating systems with low
post-copulatory selection. Numbers in parentheses, in order, are the numbers of 1) male pelvic
bone pairs, 2) male rib pairs, 3) female pelvic bone pairs, and 4) female ribs. Representative
images of the species (not to scale) were illustrated by Carl Buell, used courtesy of John Gatesy.
Images (not to scale) to the far right represent the pelvic bones and ribs for those species.
152

Figure 5.4. The correlation of residual testis mass and residual penis length in baleen whales.
Across 10 species of baleen whales, species with relatively large testes also have relatively long
penises. To account for phylogenetic affinity of the 10 baleen whales species, data presented in
Brownell and Ralls (1986) was re-analyzed as described in the Methods section. First, the
residual of penis length vs. body mass and the residual of testis mass vs. body mass were
153

calculated within a phylogenetic framework. Then another phylogenetic regression was
calculated (above) to test the correlation of residual testis mass and residual penis length.

154

Figure 5.5. Correlation of maximum testes mass and maximum body length. For 40 cetacean
species, the maximum testes mass (combined weight of left and right testes) recorded for each
species was regressed onto the maximum body length recorded for each species. The
regression was drawn with a correlation structure that accounted for phylogenetic relatedness
155

based on the molecular tree of McGowen et al. (2009). The phylogenetic residuals were used as
a metric of relative testes size.

156

Figure 5.6. Correlation of pelvic bone centroid size and maximum body length. For the 23
cetacean species for which sexually mature specimens were available, the average pelvic bone
centroid size was calculated and then regressed onto maximum body length for those species.
The regression was calculated within a phylogenetic framework account for phylogenetic
157

affinity based on the molecular tree of McGowen et al. (2009). The resulting phylogenetic
residuals were used as a metric of relative pelvic bone size.

158

Figure 5.7. Correlation of pelvic bone centroid size residuals and testes mass residuals. The
regression between testes mass residuals (taken from Fig. 5.5) and pelvic bone centroid size
residuals (taken from Fig. 5.6) was calculated within a correlation structure that accounted for
phylogenetic relatedness and intraspecific variation. Pelvic bone centroid size residuals were
significantly correlated with testes mass residuals (p=0.0012).
159

Figure 5.8. Size and shape evolution of pelvic bones and ribs in relation to testes mass. (A) All
1000 correlation coefficients sampled from the marginal posterior distributions showed that
shifts in relative testes mass positively predicted shifts in pelvic bone centroid size. (B) Shifts in
relative testes mass did not predict shifts in rib centroid size. (C) Pelvic bone shape divergence
was positively correlated with divergence in testes residuals (p = 0.008, r = 0.81). (D) Rib shape
160

divergence was not correlated with divergence in testes residuals (p = 0.72, r = 0.14). Light gray
circles show pairwise contrasts for all species. Black numbers indicate the 9 independent
species pairs for which both pelvic bones and both ribs were available (see text for description
of species pairs).

161

Figure 5.9. Marginal posterior distribution of correlation coefficients. For adult male
specimens of the comprehensive data set (i.e., not all ribs were available). Under a phylogenetic
model of correlated trait evolution, the size of the pelvic bone is positively correlated with
shifts towards larger testes after accounting for body size evolution (red), while rib bone size
does not show this correlation (gray). There is also no correlation between rib and pelvic bone
size (blue).

162

Figure 5.10. Marginal posterior distribution of correlation coefficients. For adult male
specimens for which data was available on pelvic bones and ribs. As observed for the
comprehensive data set for males (Fig. 5.9), the size of the pelvic bone is positively correlated
with shifts towards larger testes after accounting for body size evolution (red), while rib size
does not show this correlation (gray). There is also no correlation between rib and pelvic bone
size (blue).
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Figure 5.11. The marginal posterior distribution of correlation coefficients. For adult female
specimens. As in males (Figs. 5.9, 5.10), the marginal posterior distributions of correlations
between changes in female pelvic bone size was significantly correlated with shifts towards
larger testis size. The size of the pelvic bone is positively correlated with shifts towards larger
testes after accounting for body size evolution (red), while rib bone size does not show this
correlation (gray). There is also no correlation between rib and pelvic bone size (blue).
164

Table 5.1. Morphological parameters. Life history data was compiled from published sources
for 42 cetacean species. Body length is in centimeters; body mass and testes mass is in grams.
species
max
body
length
maximum
body mass
maximum
testes
mass
references
Balaena mysticetus 1800 90000000 163000.0

Burns et al. (1993)
Balaenoptera acutorostrata 880 9200000 8800.0

Tomilin (1967)
Balaenoptera borealis 1520 NA 16400.0

Perry et al. (1999)
Balaenoptera edeni 1500 40000000 20000.0

Tomilin (1967)
Balaenoptera musculus 2700 150000000 70000.0

Tomilin (1967)
Balaenoptera physalus 2400 90000000 58300.0

Jefferson et al. (2008)
Caperea marginata 550 NA 1900.0

Baker (1985)
Cephalorhynchus
commersonii
174 86000 930.0

Goodall (1994)
Delphinus capensis 250 235000 3785.0

Jefferson et al. (2008),
Ross (1979)
Delphinus delphis 270 200000 5000.0

Jefferson et al. (2008)
Eschrichtius robustus 1500 45000000 67500.0

Tomilin (1967)
Eubalaena australis 1700 90000000 972000.0

Best et al. (2001)
Eubalaena glacialis 1700 90000000 972000.0

Best et al. (2001)
Feresa attenuata 264 225000 754.0

Jefferson et al. (2008)
Globicephala
macrorhynchus
700 3600000 7000.0

Jefferson et al. (2008)
Globicephala melas 670 2320000 12300.0

Jefferson et al. (2008),
Desportes et al. (1993)
Grampus griseus 383 500000 10600.0

Jefferson et al. (2008),
Perrin and Reilly (1984)
Inia geoffrensis 255 207000 1600.0

Jefferson et al. (2008),
Best and da Silva
(1989)
Kogia breviceps 425 417000 10000.0

Tomilin (1994),
Bloodworth and Odell
(2008), Caldwell et al.
(1971), Ruiz (1993)
Kogia sima 270 280000 2618.0

Ross (1979)
Lagenorhynchus acutus 280 235000 740.0

Jefferson et al. (2008)
Lagenorhynchus obliquidens 250 200000 1118.0

Harrison et al. (1972)
165

species
max
body
length
maximum
body mass
maximum
testes
mass
References
Lissodelphis borealis 307 115000 1410.0

Harrison et al. (1972)
Megaptera novaeangliae 1700 40000000 4000.0

Jefferson et al. (2008)
Mesoplodon carlhubbsi 540 1500000 510.0
Jefferson et al. (2008),
Mead et al. (1982)
Monodon monoceros 480 1600000 NA

Jefferson et al. (2008)
Neophocaena phocaenoides 200 55000 863.0

Kasuya (1999)
Orcinus orca 975 10000000 23100.0

Jefferson et al. (2008),
Ross (1979)
Peponocephala electra 278 275000 4500.0

Jefferson et al. (2008)
Phocoena phocoena 180 61000 3515.0

Read (1999)
Phocoenoides dalli 240 200000 560.0

Jefferson et al. (2008)
Physeter macrocephalus 1800 57000000 12000.0

Jefferson et al. (2008)
Pontoporia blainvillei 160 50000 10.8

Jefferson et al. (2008)
Pseudorca crassidens 600 2000000 14800.0

Jefferson et al. (2008)
Stenella attenuata 257 120000 2896.0

Jefferson et al. (2008),
Hohn et al. (1985)
Stenella coeruleoalba 256 160000 500.0

Miyazaki (1977)
Stenella frontalis 230 140000 1210.0

Perrin et al. (1994)
Stenella longirostris 235 82000 2708.0

Jefferson et al. (2008)
Steno bredanensis 265 160000 2660.0

Miyazaki and Perrin
(1994)
Tursiops aduncus 270 230000 NA

Wells and Scott (1999)
Tursiops truncatus 381 650000 1966.0

Perrin and Reilly (1984)
Ziphius cavirostris 700 3000000 4200.0 Omura et al. (1955)
166

Table 5.2. Specimens examined. 134 specimens comprising 27 species were obtained from
museum collections. Centroid size data is listed for individual pelvic bones and ribs (NA
indicates the bone was not available). Museum source is indicated in the SPECIMEN ID column
(BMNH=British Museum of Natural History; CCSN=Cape Cod Stranding Network; LACM=Natural
History Museum of Los Angeles County; MAL=Marine Animal Life; MH=New England Aquarium;
MJM=Michael J. Moore; UMA=University of Massachusetts, Amherst; USNM=United States
National Museum of Natural History (Smithsonian Inst.); UWBM=University of Washington
Burke Museum).
SPECIES SPECIMEN ID SEX
BODY
LENGTH
PELVIC
LEFT
PELVIC
RIGHT
RIB
LEFT
RIB
RIGHT
Balaenoptera
acutorostrata
MAL 03-282 F 730 2299.8 2246.1 NA NA
Balaenoptera
acutorostrata
MH 03-621 M 700 1898.3 1868.0 NA NA
Balaenoptera musculus
BMNH 1953-
12.1.18
F 2350 3862.8 3771.2 NA NA
Balaenoptera musculus
BMNH 1953-
12.1.19
M 2360 3765.0 NA NA NA
Balaenoptera physalus LACM 31144 U 2135 3648.4 3649.3 NA NA
Balaenoptera physalus UMA 4820 F 2075 2376.7 2405.2 NA NA
Delphinus capensis LACM 84071 M 209 860.0 858.7 1221.3 1264.7
Delphinus capensis LACM 84127 M 215 736.7 737.6 1222.2 1243.3
Delphinus capensis LACM 84163 M 226 796.7 808.0 1473.7 1458.9
Delphinus capensis LACM 84185 M 211.5 907.7 898.7 1276.7 1346.0
Delphinus capensis LACM 84220 M 212 851.6 870.7 1361.0 1347.5
Delphinus capensis LACM 84221 M 218.5 853.1 840.8 1418.8 1442.4
Delphinus capensis LACM 84233 M 223.5 963.6 943.7 1280.4 1302.6
Delphinus capensis LACM 84236 F 208 677.1 695.4 1210.3 1227.1
Delphinus capensis LACM 84239 M 208.5 670.5 657.6 1356.7 1357.9
Delphinus capensis LACM 84240 M 235 884.6 868.9 1420.8 1429.1
Delphinus capensis LACM 84241 M 232.9 892.4 937.8 NA NA
Delphinus capensis LACM 85995 M 210 896.8 894.2 1463.8 1429.0
Delphinus capensis LACM 86004 M 233 853.4 892.7 1454.6 1450.5
Delphinus capensis LACM 88979 M 211.5 902.6 903.3 1293.9 1297.8
Delphinus capensis LACM 88999 M 214 730.3 735.1 NA NA
Delphinus capensis LACM 91307 F 207 915.7 906.7 1270.0 1271.4
Delphinus capensis LACM 91779 M 234 854.5 860.3 1306.3 1289.7
167

SPECIES SPECIMEN ID SEX
BODY
LENGTH
PELVIC
LEFT
PELVIC
RIGHT
RIB
LEFT
RIB
RIGHT
Delphinus capensis LACM 91915 M 222 895.8 928.2 1345.6 1360.4
Delphinus capensis LACM 92071 M 227 939.3 947.4 1454.0 1518.5
Delphinus capensis LACM 92077 M 222.5 987.2 1021.4 1342.3 1433.3
Delphinus capensis LACM 95668 M 218 NA NA 1271.4 1241.8
Delphinus capensis LACM 96366 M 217.5 860.1 825.2 1382.1 1351.8
Delphinus capensis LACM 97203 M 219 NA 653.3 NA NA
Delphinus capensis LACM 97204 M 224 807.2 838.9 NA NA
Delphinus capensis LACM 97429 M 232 987.3 956.3 1477.3 1506.3
Delphinus capensis LACM 97478 M 212 851.8 855.3 1460.5 1455.7
Delphinus delphis LACM 84254 M 229 938.2 915.4 1395.5 1391.7
Delphinus delphis USNM 504107 M 209 989.3 996.2 1379.4 706.2
Delphinus delphis USNM 572632 M 223 870.3 852.7 NA 1357.1
Delphinus delphis USNM 572775 M 203 1097.2 1097.6 1361.3 1434.8
Delphinus delphis USNM 572776 M 228 983.2 991.2 1388.7 1388.4
Delphinus delphis USNM 572777 M 216 922.4 924.3 1305.4 1426.2
Delphinus delphis USNM 572859 F 207 820.8 839.3 1357.6 1347.0
Delphinus delphis USNM 572871 M 229 NA 1051.0 1311.3 1283.7
Delphinus delphis USNM 572980 M 225 1028.1 1016.2 1449.1 1387.5
Eschrichtius robustus UWBM 35430 M 1293 4557.0 NA NA NA
Eubalaena glacialis MJM 070110 M 1370 4305.6 4471.8 NA NA
Eubalaena glacialis UMA 4920 F 1370 3432.7 3395.9 NA NA
Feresa attenuata LACM 84252 M 214 1082.9 1090.3 1334.6 1345.3
Feresa attenuata USNM 550389 M 212 1049.2 1049.8 NA 1351.9
Feresa attenuata USNM 571268 M 230 993.6 1001.5 1517.2 1522.4
Globicephala melas CCSN 04-141 F 460 1306.4 1175.8 NA NA
Grampus griseus LACM 72546 M 360.7 1208.7 1192.7 2347.2 2380.0
Grampus griseus USNM 504126 M 298 1125.2 1107.5 1976.2 2007.2
Grampus griseus USNM 550391 M 286 988.5 1020.2 1926.1 1922.7
Inia geoffrensis LACM 19590 M 240 988.5 1013.9 1462.4 1493.0
Inia geoffrensis LACM 27074 M 228 940.7 898.0 1567.9 1641.4
Lagenorhynchus acutus USNM 504154 F 234.5 860.0 853.9 1580.8 1562.2
Lagenorhynchus acutus USNM 550995 M 253 959.1 995.1 1618.7 1610.3
Lagenorhynchus acutus USNM 571327 M 253 843.3 907.9 1578.4 1588.3
Lagenorhynchus acutus USNM 571390 M 242 968.0 978.3 1550.5 1566.8
168

SPECIES SPECIMEN ID SEX
BODY
LENGTH
PELVIC
LEFT
PELVIC
RIGHT
RIB
LEFT
RIB
RIGHT
Lagenorhynchus
obliquidens
LACM 84284 M 220 902.3 967.9 1572.0 1517.1
Lagenorhynchus
obliquidens
LACM 88951 M 192 885.5 856.2 1528.5 1465.4
Lagenorhynchus
obliquidens
LACM 88987 M 207 771.8 778.0 1475.7 1454.0
Lagenorhynchus
obliquidens
LACM 92062 M 194 733.2 757.2 1386.8 1417.4
Lagenorhynchus
obliquidens
LACM 95514 F 223 765.2 717.1 1588.5 1686.0
Lissodelphis borealis LACM 72455 M 264.4 999.8 1010.6 1343.2 1358.5
Lissodelphis borealis LACM 95689 M 217.8 974.3 987.5 1161.6 1245.6
Lissodelphis borealis USNM 484929 M 265.3 1128.5 1139.6 1489.9 1536.7
Mesoplodon carlhubbsi USNM 504128 F 532 1007.1 1043.3 3119.4 3124.1
Peponocephala electra LACM 54090 F 231 1008.1 974.6 1611.4 1635.9
Phocoena phocoena LACM 72591 M 148 1063.1 1058.3 NA NA
Phocoena phocoena LACM 84072 M 154 1018.1 995.4 1491.8 1475.3
Phocoena phocoena LACM 84073 F 173 829.5 872.4 1403.8 1414.0
Phocoena phocoena LACM 84076 F 178 945.3 997.7 1409.8 1415.6
Phocoena phocoena LACM 84086 F 164.5 880.5 877.0 1319.0 1317.5
Phocoena phocoena USNM 504302 F 165 834.4 917.4 1275.9 1279.1
Phocoena phocoena USNM 550042 U 149 1161.8 NA 1335.7 1316.9
Phocoena phocoena USNM 550312 F 158 897.4 879.9 1334.4 1362.6
Phocoena phocoena USNM 571709 M 160.2 1155.7 1159.7 1409.4 1352.6
Phocoena phocoena USNM 571723 M 146.1 1094.4 1086.9 1125.8 1152.4
Phocoena phocoena USNM 572629 F 163 718.3 775.9 1361.7 1374.8
Phocoena phocoena USNM 572785 M 151.5 1108.1 1110.9 1299.1 1328.9
Phocoenoides dalli LACM 54420 M 203 793.8 846.7 1679.6 1600.2
Phocoenoides dalli LACM 54569 F 200 690.3 695.7 1748.3 1747.2
Phocoenoides dalli LACM 84048 M 213 590.0 575.1 1568.3 1510.1
Phocoenoides dalli LACM 84251 M 225 686.9 733.8 1749.3 1753.2
Phocoenoides dalli LACM 96383 M 213.5 770.1 777.2 1556.0 1514.2
Phocoenoides dalli LACM 96487 M 210 557.9 NA NA NA
Phocoenoides dalli LACM 97207 M 210 691.5 677.9 NA NA
Phocoenoides dalli USNM 396304 M 202 795.3 794.9 1567.3 1566.4
Pontoporia blainvillei LACM 47143 M 128.5 302.0 297.5 774.5 803.6
169

SPECIES SPECIMEN ID SEX
BODY
LENGTH
PELVIC
LEFT
PELVIC
RIGHT
RIB
LEFT
RIB
RIGHT
Pontoporia blainvillei LACM 54012 F 138 396.6 364.7 848.7 861.0
Pontoporia blainvillei USNM 501157 F 136 343.5 325.3 833.2 842.3
Pontoporia blainvillei USNM 501172 M 137 NA NA 720.1 764.6
Pontoporia blainvillei USNM 501176 F 142 340.0 343.2 798.8 846.6
Pontoporia blainvillei USNM 501179 M 142 407.2 428.4 797.5 834.9
Pontoporia blainvillei USNM 501183 F 145 285.2 295.8 828.4 883.0
Pontoporia blainvillei USNM 501186 F 143 355.9 288.3 793.3 794.0
Pontoporia blainvillei USNM 504920 F 155 490.4 443.4 880.8 911.0
Pseudorca crassidens LACM 84047 M 480 1379.1 1362.4 2352.0 2415.8
Stenella attenuata LACM 54043 M 195 651.2 628.4 1144.1 1155.2
Stenella attenuata LACM 95489 F 191.9 572.8 545.6 1157.5 1170.1
Stenella attenuata USNM 395277 F 175 646.1 643.2 NA NA
Stenella attenuata USNM 395390 M 218 722.1 707.3 1112.3 1128.2
Stenella attenuata USNM 395465 M 200 759.0 712.4 1116.3 NA
Stenella coeruleoalba USNM 504350 M 231 737.4 740.6 1473.1 1459.4
Stenella coeruleoalba USNM 504773 M 221.7 669.9 662.8 1564.6 1532.2
Stenella frontalis USNM 504758 M 201 742.5 736.4 1434.6 1462.4
Stenella longirostris LACM 72437 M 175.4 541.2 579.8 1009.1 975.9
Stenella longirostris LACM 72438 M 177.5 651.7 664.0 1179.8 1198.3
Stenella longirostris USNM 395599 M 173 692.4 702.7 1161.8 1157.9
Steno bredanensis USNM 504467 M 235 737.0 761.0 NA 1672.7
Steno bredanensis USNM 504468 M 227 745.8 741.6 NA 1628.7
Steno bredanensis USNM 504494 M 233 748.6 818.3 NA 1393.5
Steno bredanensis USNM 550837 M 228.1 787.4 780.2 1538.6 1488.7
Tursiops aduncus USNM 258642 M 287 905.2 914.7 1900.4 1927.8
Tursiops truncatus LACM 84194 M 304 1108.3 1156.8 1827.2 1876.1
Tursiops truncatus LACM 84267 M 305 865.6 868.1 1941.6 1838.3
Tursiops truncatus LACM 84271 F 285 663.1 616.9 1720.5 1704.1
Tursiops truncatus LACM 92072 M 288 746.3 717.5 1768.1 1785.2
Tursiops truncatus LACM 95828 M 293 959.0 939.2 NA NA
Tursiops truncatus LACM 97405 F 277 842.1 955.1 1705.4 1709.0
Tursiops truncatus LACM 97489 F 298 1083.8 1045.8 1817.7 1914.5
Tursiops truncatus USNM 396165 M 303 796.7 876.0 1911.5 NA
Tursiops truncatus USNM 504726 M 298 1068.1 1094.0 2014.3 1940.9
Tursiops truncatus USNM 504879 M 284 1000.5 1000.5 NA 1874.6
170

SPECIES SPECIMEN ID SEX
BODY
LENGTH
PELVIC
LEFT
PELVIC
RIGHT
RIB
LEFT
RIB
RIGHT
Tursiops truncatus USNM 550401 M 267.5 1073.7 1046.9 1701.2 1697.5
Tursiops truncatus USNM 550422 M 279 1155.2 1150.8 1812.2 1782.7
Tursiops truncatus USNM 550919 F 283 953.6 966.2 1833.0 1810.8
Tursiops truncatus USNM 571051 M 277 999.0 1024.7 1766.0 1763.1
Tursiops truncatus USNM 571086 M 273 1078.9 1030.9 1644.9 1723.9
Tursiops truncatus USNM 571388 F 285 790.6 830.5 1491.6 1509.5
Tursiops truncatus USNM 571521 M 271 659.5 669.7 1399.0 1396.5
Tursiops truncatus USNM 572949 M 265 1166.0 1105.4 1697.1 1644.7
Tursiops truncatus USNM 593406 M 279 1167.8 1172.6 1736.8 1770.7
Ziphius cavirostris USNM A20971 F 589 854.0 828.4 3676.2 3580.3
Ziphius cavirostris USNM A49599 M 564 978.7 1067.3 4095.2 3972.7

171

Table 5.3. Posterior means and quantiles of the parameters of the model presented in
equations (7) and (8). Results are from all adult male specimens.

σ
L
β
T
β
P
β
R
σ
R
σ
P
ς
L
ς
R

5% 0.11 0.38 0.03 -0.02 0.03 0.05 0.04 0.06
25% 0.14 0.45 0.05 -0.01 0.03 0.06 0.04 0.07
mean 0.55 0.55 0.07 0.00 0.04 0.07 0.04 0.07
75% 0.51 0.61 0.08 0.01 0.05 0.07 0.05 0.07
95% 2.28 0.88 0.11 0.03 0.06 0.09 0.05 0.08

ω
R
ς
P
ω
P
δ
T
δ
R
δ
P
η
P
η
R

5% 0.04 0.10 0.01 0.08 0.09 0.05 0.02 -0.00
25% 0.04 0.11 0.02 0.27 0.27 0.08 0.08 0.01
mean 0.04 0.12 0.02 1.60 1.60 0.47 0.47 0.02
75% 0.04 0.13 0.02 3.29 3.29 0.54 0.54 0.02
95% 0.05 0.14 0.02 4.27 4.27 1.99 1.99 0.04

172

Table 5.4. Marginal posterior distributions of correlations, with fixed length, between changes
in rib size, pelvic bone size, and testes size, estimated using only bones from sexually mature
males.
testes-ribs testes-pelvics ribs-pelvics
Min. -0.8087000 0.0594300 -0.7689000
2.5% -0.5075804 0.2476295 -0.3776489
1st Qrtl. -0.1367000 0.5748000 -0.0833000
Median 0.0759300 0.7001000 0.0432000
Mean 0.0665400 0.6682000 0.0461500
3rd Qrtl. 0.2769000 0.7872000 0.1720000
97.5% 0.6225153 0.9025416 0.4816755
Max. 0.8719000 0.9694000 0.8116000

173

Table 5.5. Posterior means and quantiles of the parameters of the model presented in
equations (7) and (8). Results are from all adult male specimens for which both pelvic bones
and ribs were available.

σ
L
β
T
β
P
β
R
σ
R
σ
P
ς
L
ς
R

5% 0.22 0.42 0.01 -0.02 0.03 0.05 0.04 0.06
25% 0.04 0.50 0.05 -0.01 0.03 0.07 0.04 0.07
mean 1.08 0.63 0.08 0.00 0.04 0.10 0.04 0.07
75% 1.74 0.71 0.11 0.01 0.05 0.12 0.05 0.07
95% 2.07 0.98 0.17 0.03 0.06 0.16 0.05 0.08

ω
R
ς
P
ω
P
δ
T
δ
R
δ
P
η
P
η
R

5% 0.04 0.10 0.01 1.59 0.66 0.80 0.55 -0.04
25% 0.04 0.11 0.02 1.88 0.77 1.09 0.70 0.15
mean 0.04 0.12 0.02 2.50 0.86 1.32 0.82 0.30
75% 0.04 0.13 0.02 5.55 0.93 1.51 0.93 0.45
95% 0.05 0.14 0.02 7.95 1.03 1.87 1.01 0.64

174

Table 5.6. Marginal posterior distributions of correlations, with fixed length, between changes
in rib size, pelvic bone size, and testes size, estimated using only bones from sexually mature
males with complete pelvic bones and ribs.

testes-ribs testes-pelvics ribs-pelvics
Min. -0.7011000 -0.3474000 -0.5741000
2.5% -0.5280824 -0.0463272 -0.3928919
1st Qrtl. -0.1584000 0.4258000 -0.0787800
Median 0.0371700 0.6312000 0.0126700
Mean 0.0605700 0.5849000 0.0372300
3rd Qrtl. 0.2918000 0.7870000 0.1450000
97.5% 0.6390835 0.9244852 0.4975437
Max. 0.8554000 0.9698000 0.7611000

175

Table 5.7. Posterior means and quantiles of the parameters of the model presented in
equations (7) and (8). Results are from adult female specimens.

σ
L
β
T
β
P
β
R
σ
R
σ
P
ς
L
ς
R

5% 0.13 0.39 0.03 -0.02 0.02 0.02 0.03 0.04
25% 0.02 0.46 0.04 0.00 0.03 0.03 0.03 0.05
mean 0.18 0.54 0.06 0.01 0.03 0.04 0.03 0.06
75% 0.20 0.60 0.07 0.02 0.04 0.05 0.03 0.06
95% 0.25 0.76 0.10 0.03 0.06 0.07 0.04 0.06

ω
R
ς
P
ω
P
δ
T
δ
P
η
P
δ η
R

5% 0.01 0.11 0.03 0.07 0.74 -0.16 0.30 -0.55
25% 0.01 0.13 0.03 0.98 0.88 0.26 0.47 0.28
mean 0.01 0.15 0.03 1.76 0.97 0.49 0.57 1.04
75% 0.01 0.16 0.04 2.49 1.05 0.76 0.68 1.74
95% 0.02 0.18 0.04 3.46 1.20 1.08 0.84 2.84

176

Table 5.8. Marginal posterior distributions of correlations, with fixed length, between changes
in rib size, pelvic bone size, and testes size, estimated using only bones from sexually mature
females.

testes-ribs testes-pelvics ribs-pelvics
Min. -0.8225000 -0.2529000 -0.8156000
2.5% -0.5799271 0.3004328 -0.4842241
1st Qrtl. -0.0687000 0.6983000 -0.0452200
Median 0.2468000 0.8280000 0.1670000
Mean 0.2027000 0.7789000 0.1576000
3rd Qrtl. 0.4903000 0.9067000 0.3738000
97.5% 0.7967721 0.9914113 0.6948937
Max. 0.9369000 0.9998000 0.8510000

177

Table 5.9. Distance-based ANOVA of pairwise differences in pelvic bone centroid size.
Results are from a nested ANOVA performed on the pairwise distance matrix of
relative pelvic bone centroid size (pelvic bone centroid size divided by body length).

Level Df Sums of Sqs Mean Sqs F.Model r
2
Pr(>F)
species 27 258.14 9.56 945.02 0.81 0.00
sex 15 27.20 1.81 179.25 0.08 0.00
specimen 89 33.68 0.38 37.40 0.11 0.00
Residuals 126 1.27 0.01 0.00
Total 257 320.30 1.00

178

Table 5.10. Distance-based ANOVA of pairwise differences in rib size. Results are from
a nested ANOVA performed on the pairwise distance matrix of relative rib centroid size
(rib centroid size divided by body length).

Level Df Sums of Sqs Mean Sqs F.Model r
2
Pr(>F)
species 21 141.95 6.76 103.64 0.78 0.00
sex 11 6.69 0.61 9.33 0.04 0.00
specimen 82 26.07 0.32 4.88 0.14 0.00
Residuals 107 6.98 0.07 0.04
Total 221 181.69 1.00

179

Table 5.11. Distance-based ANOVA of pairwise differences in pelvic bone shape.
Results are from a nested ANOVA performed on the Procrustes distance matrix for
pelvic bones.

Level Df Sums of Sqs Mean Sqs F.Model r
2
Pr(>F)
species 27 0.18 0.01 15.57 0.34 0.00
sex 15 0.07 0.00 11.18 0.14 0.00
specimen 89 0.21 0.00 5.78 0.42 0.00
Residuals 126 0.05 0.00 0.10
Total 257 0.51 1.00

180

Table 5.12. Distance-based ANOVA of pairwise differences in rib shape. Results from a
nested ANOVA performed on the Procrustes distance matrix for ribs.

Level DF Sums of Sqs Mean Sqs F.Model r
2
Pr(>F)
species 21 0.09 0.00 18.72 0.45 0.00
sex 11 0.01 0.00 4.93 0.06 0.00
specimen 82 0.07 0.00 3.83 0.36 0.00
Residuals 107 0.02 0.00 0.12
Total 221 0.20 1.00

181

Chapter 6 – Conclusions

Contrary to widely established interpretation, the pelvic bones of modern cetaceans are
not useless vestiges. Although these structures no longer support functional hind limbs, they do
play an important role in reproduction. Pelvic bones are anchors for the organs of the
reproductive system. The main body of the cetacean penis bifurcates proximally into two crura,
each of which attaches to its own pelvic bone. Paired muscles associated with the penis, the
erector penis (also known as the ischiocavernosus) muscles, also originate on a pelvic bone. The
female analog, the clitoris and erector clitoridis muscles, are similarly situated. Although the
pelves of all tetrapods anchor the genitalia, the evolutionary transition of cetaceans from a
quadrupedal and terrestrial existence to a fully aquatic mode of life means that the primary
function of cetacean pelvic bones is one of mating. Thus, cetacean pelvic bones are uniquely
suited to test the influence of sexual selection on their morphology.
One of the most striking features of cetacean pelvic bones is their morphologic
variability, a characteristic that conforms to sexual selection theory. The rapid divergent
evolution of male genitalia, for example, is one of the most general evolutionary trends in
animals with internal fertilization (Arnqvist 1998). It follows that pelvic bones—structures that
in cetaceans only function to support the genitalia—would be influenced by the same
evolutionary dynamics. The driving force behind sexual selection is differential mating success,
wherein slight modifications in reproductive structures lead to advantages in securing mating
opportunities and successful fertilizations. Sexual selection emerges from the struggle to
182

reproduce and results in myriad minor variations, like those observed in the pelvic bones of
cetaceans.
The interspecific variation in pelvic bones among cetaceans can be conspicuous, with
species having a similar body size possessing pelvic bones dramatically different in size and
shape. For example, a 1.9 meter long adult male harbor porpoise (Phocoena phocoena) may
have pelvic bones up to 11 centimeters in length, while the pelvic bones from an adult male of
the related but slightly longer Dall’s porpoise (Phocoenoides dalli) reach only up to about 7
centimeters. Verified data are lacking, but harbor porpoises anecdotally have penises up to 1/3
their body length. Penis length in Dall’s porpoise is unknown. It makes sense that having a
longer penis necessitates larger, more robust pelvic bones.
In Chapter 4, data from Brownell and Ralls Brownell and Ralls (1986) were re-analyzed in
a phylogenetic context, showing a positive correlation between relative testes mass and
relative penis length in baleen whales. We saw in Chapter 3 that relative testes mass is a good
proxy for mating strategy; species with large relative testes mass experience intense sperm
competition, as occurs in promiscuous mating systems. Among the baleen whales included in
the analyses presented within, the species with the largest relative testes also had the largest
pelvic bones. Thus, large relative testes = large relative penis = large pelvic bones.
Large relative testes size in promiscuous mating systems is typically explained by the
presence of sperm competition, where the sperm of two or more males are competing within a
female’s reproductive tract for a successful fertilization. To the extent that larger testes can
produce more sperm, potentially flushing out the sperm of rival males, having larger testes can
183

pay off. The adaptive significance of a longer penis in promiscuous mating systems is less easily
explained. Does having a longer penis allow the male to position his sperm closer to the cervix
than sperm from a competing male? Or perhaps a longer penis allows the male to overcome
female resistance behavior. Yet another possibility is that a longer penis is a response to cryptic
female choice (Eberhard 1996). Harrison (1949) noted the complicated reproductive tract in
female long-finned pilot whales (Globicephala melas), with convoluted muscular folds that
potentially act as pseudo-cervices to prevent insemination by unwanted males. One avenue of
future research is a comprehensive anatomical study of female reproductive tracts across
Cetacea to test, for example, correlations between a species’ mating strategy and the nature of
the female reproductive tract.
A curious finding in this study was the “re-discovery” of the absence of ossified pelvic
bones in two species: the pygmy and dwarf sperm whales (Kogia breviceps and K. sima,
respectively). The absence of ossified pelvic bones in kogiids was originally described by
Benham (1901a; 1902), but remains unknown to many contemporary cetologists. Although
disappearance of ossified structures might appear to support the idea that pelvic bones are on
an evolutionary tract of being lost, they clearly are an exception to the rule. Dense sheets of
cartilaginous tissue have replaced the ossified pelvic bones (Schulte and Smith 1918) and have
assumed the function of anchoring function the genitalia. This unique feature of kogiids may
actually be an example of neoteny. Pelvic bones are typically still cartilaginous at birth, not
becoming fully ossified until sexual maturity (Hosokawa 1951; Andersen et al. 1992). Unossified
pelvic “bones” in kogiids may simply be retention of a juvenile characteristic, but further study
is needed to confirm this hypothesis.
184

Another avenue of future research is taking an evolutionary developmental approach to
the study of hind limb anatomy in cetaceans. Integrating paleontological data with the causal
study of developmental mechanisms can lend insights into the evolutionary origin and
transformation of structures like fins and limbs (Brigandt 2009). For example, in comparing the
fossil pelvic bones from a Miocene whale to pelvic bones from modern whales, Gol'din (2014)
suggested that all the three elements comprising the traditional mammalian pelvis (i.e., ilium,
ischium and pubis) also comprise the modern cetacean pelvic bones. As discussed in the
present study, this condition may be true for baleen whales (Gol’din apparently only included
baleen whales in his analysis), but is not likely true for the toothed whales. Embryological
studies and continued work on control genes has the potential to provide clarification on issues
like this. Harnessing technologies such as high-resolution CT scanning to examine series of
cetacean embryos available in collections also shows promise.
Clearly, some work remains to be done to elucidate the evolutionary processes that
have shaped hind limb and pelvic bone structure in modern cetaceans, but the results
presented here significantly change our understanding of those evolutionary processes. First,
the textbook examples of cetacean pelvic being useless vestiges are incorrect. By functioning as
anchors for the genitalia and associate muscles, the pelvic bones in living whales and dolphins
play a crucial role in reproduction. Moreover, when cetacean pelvic bones lost their function in
supporting hindlimbs, it became possible for sexual selection to influence their evolution.
Under that influence, a species’ mating ecology determines the size and shape of the pelvic
bones. Pelvic bone size is correlated with the intensity of sperm competition a species
experiences, as inferred from relative testes mass. The larger the relative testes mass, the more
185

sperm competition occurring and the greater the pelvic bone size. Similarly, shape of pelvic
bones in cetaceans varies more with increased relative testes mass. Species with larger relative
testes mass also have more divergent pelvic bone shape.

186

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220

Appendix: Specimens Examined
Catalog Number Species Sex
Body
Length
Age Family
BMNH 1920.5.4.7 Balaenoptera musculus M U U Balaenopteridae
BMNH
1953.12.1.15
Balaenoptera musculus U U U Balaenopteridae
BMNH
1953.12.1.18
Balaenoptera musculus F 2350 A Balaenopteridae
BMNH
1953.12.1.19
Balaenoptera musculus M 2360 A Balaenopteridae
BMNH
1953.12.1.21
Physeter macrocephalus M 1540 J Physeteridae
BMNH
1953.12.1.23
Physeter macrocephalus U U U Physeteridae
BMNH 1953.12.1.9 Eubalaena australis U U U Balaenidae
CAS 28860 Balaenoptera musculus F U U Balaenopteridae
CAS 29766 Megaptera novaeangliae F 1196 J Balaenopteridae
CAS 7267 Balaenoptera musculus U U U Balaenopteridae
CAS 9833 Mesoplodon sp. U U U Ziphiidae
CCSN 04-141 Globicephala melas F 460 A Delphinidae
CCSN 04-152 Balaenoptera
acutorostrata
F 650 J Balaenopteridae
CCSN 04-224 Megaptera novaeangliae F 1280 J Balaenopteridae
CM 60934 Inia geoffrensis F U U Iniidae
CM 60936 Inia geoffrensis F U U Iniidae
HSU 2681 Phocoena phocoena M U U Phocoenidae
HSU 2682 Phocoena phocoena F U U Phocoenidae
HSU 2716 Neophocaena
phocaenoides
U U U Phocoenidae
HSU 2717 Peponocephala electra U U U Delphinidae
IFAW 09-018 Balaenoptera physalus M 1220 J Balaenopteridae
IFAW 10-188 Megaptera novaeangliae M 914 J Balaenopteridae
LACM 19590 Inia geoffrensis M 240 A Iniidae
LACM 27064 Inia geoffrensis U U U Iniidae
LACM 27074 Inia geoffrensis M 228 A Iniidae
LACM 27079 Tursiops truncatus M 148 J Delphinidae
LACM 27094 Tursiops truncatus F 227 J Delphinidae
LACM 27434 Stenella attenuata U U U Delphinidae
LACM 28257 Inia geoffrensis U U U Iniidae
LACM 31144 Balaenoptera physalus U 2135 A Balaenopteridae
LACM 31447 Feresa attenuata M U U Delphinidae
LACM 47143 Pontoporia blainvillei M 129 A Pontoporidae
221

Catalog Number Species Sex
Body
Length
Age Family
LACM 54012 Pontoporia blainvillei F 138 A Pontoporidae
LACM 54042 Stenella attenuata F 170 J Delphinidae
LACM 54043 Stenella attenuata M 195 A Delphinidae
LACM 54083 Lissodelphis borealis M 232 J Delphinidae
LACM 54090 Peponocephala electra F 231 A Delphinidae
LACM 54109 Phocoenoides dalli M 194 A Phocoenidae
LACM 54420 Phocoenoides dalli M 203 A Phocoenidae
LACM 54569 Phocoenoides dalli F 200 A Phocoenidae
LACM 54616 Phocoenoides dalli M U U Phocoenidae
LACM 54637 Lissodelphis borealis F U U Delphinidae
LACM 54808 Balaenoptera
acutorostrata
F U U Balaenopteridae
LACM 72176 Tursiops truncatus M 200 J Delphinidae
LACM 72437 Stenella longirostris M 175 A Delphinidae
LACM 72438 Stenella longirostris M 178 A Delphinidae
LACM 72455 Lissodelphis borealis M 264 A Delphinidae
LACM 72490 Balaena mysticetus F 1680 J Balaenidae
LACM 72531 Tursiops truncatus U U U Delphinidae
LACM 72546 Grampus griseus M 361 A Delphinidae
LACM 72548 Monodon monoceros M 472 J Monodontidae
LACM 72569 Monodon monoceros M 338 J Monodontidae
LACM 72591 Phocoena phocoena M 148 A Phocoenidae
LACM 84016 Phocoena phocoena M 130 J Phocoenidae
LACM 84040 Delphinus capensis F 189 J Delphinidae
LACM 84047 Pseudorca crassidens M 480 A Delphinidae
LACM 84048 Phocoenoides dalli M 213 A Phocoenidae
LACM 84071 Delphinus capensis M 209 A Delphinidae
LACM 84072 Phocoena phocoena M 154 A Phocoenidae
LACM 84073 Phocoena phocoena F 173 A Phocoenidae
LACM 84076 Phocoena phocoena F 178 A Phocoenidae
LACM 84083 Mesoplodon carlhubbsi M 248 J Ziphiidae
LACM 84086 Phocoena phocoena F 165 A Phocoenidae
LACM 84091 Delphinus capensis M 191 J Delphinidae
LACM 84097 Tursiops truncatus F 235 J Delphinidae
LACM 84120 Tursiops truncatus M 239 J Delphinidae
LACM 84127 Delphinus capensis M 215 A Delphinidae
LACM 84163 Delphinus capensis M 226 A Delphinidae
LACM 84185 Delphinus capensis M 212 A Delphinidae
LACM 84194 Tursiops truncatus M 304 A Delphinidae
222

Catalog Number Species Sex
Body
Length
Age Family
LACM 84200 Phocoena phocoena M 142 J Phocoenidae
LACM 84214 Phocoena phocoena M 131 J Phocoenidae
LACM 84220 Delphinus capensis M 212 A Delphinidae
LACM 84221 Delphinus capensis M 219 A Delphinidae
LACM 84223 Delphinus capensis F 196 J Delphinidae
LACM 84233 Delphinus capensis M 224 A Delphinidae
LACM 84236 Delphinus capensis F 208 A Delphinidae
LACM 84239 Delphinus capensis M 209 A Delphinidae
LACM 84240 Delphinus capensis M 235 A Delphinidae
LACM 84241 Delphinus capensis M 233 A Delphinidae
LACM 84248 Tursiops truncatus M 242 J Delphinidae
LACM 84249 Orcinus orca M 665 A Delphinidae
LACM 84251 Phocoenoides dalli M 225 A Phocoenidae
LACM 84252 Feresa attenuata M 214 A Delphinidae
LACM 84254 Delphinus delphis M 229 A Delphinidae
LACM 84256 Delphinus capensis M 198 J Delphinidae
LACM 84267 Tursiops truncatus M 305 A Delphinidae
LACM 84271 Tursiops truncatus F 285 A Delphinidae
LACM 84278 Delphinus capensis M 188 J Delphinidae
LACM 84284 Lagenorhynchus
obliquidens
M 220 A Delphinidae
LACM 84285 Tursiops truncatus F 268 J Delphinidae
LACM 85952 Stenella coeruleoalba F 217 A Delphinidae
LACM 85995 Delphinus capensis M 210 A Delphinidae
LACM 86001 Delphinus capensis M 187 J Delphinidae
LACM 86002 Delphinus delphis M 194 J Delphinidae
LACM 86004 Delphinus capensis M 233 A Delphinidae
LACM 86041 Neophocaena
phocaenoides
M 129 J Phocoenidae
LACM 88939 Delphinus capensis M 188 J Delphinidae
LACM 88951 Lagenorhynchus
obliquidens
M 192 A Delphinidae
LACM 88955 Delphinus capensis F 189 J Delphinidae
LACM 88979 Delphinus capensis M 212 A Delphinidae
LACM 88987 Lagenorhynchus
obliquidens
M 207 A Delphinidae
LACM 88999 Delphinus capensis M 214 A Delphinidae
LACM 91307 Delphinus capensis F 207 A Delphinidae
LACM 91779 Delphinus capensis M 234 A Delphinidae
LACM 91915 Delphinus capensis M 222 A Delphinidae
223

Catalog Number Species Sex
Body
Length
Age Family
LACM 92062 Lagenorhynchus
obliquidens
M 194 A Delphinidae
LACM 92071 Delphinus capensis M 227 A Delphinidae
LACM 92072 Tursiops truncatus M 288 A Delphinidae
LACM 92077 Delphinus capensis M 223 A Delphinidae
LACM 95489 Stenella attenuata F 192 A Delphinidae
LACM 95514
Lagenorhynchus
obliquidens F 223 A Delphinidae
LACM 95657 Delphinus capensis F 192 J Delphinidae
LACM 95664 Tursiops truncatus M 260 J Delphinidae
LACM 95668 Delphinus capensis M 218 A Delphinidae
LACM 95689 Lissodelphis borealis M 218 A Delphinidae
LACM 95748 Phocoena phocoena M 155 A Phocoenidae
LACM 95778 Phocoena phocoena M 134 J Phocoenidae
LACM 95811 Delphinus capensis F 194 J Delphinidae
LACM 95828 Tursiops truncatus M 293 A Delphinidae
LACM 95994 Tursiops truncatus U 267 A Delphinidae
LACM 96366 Delphinus capensis M 218 A Delphinidae
LACM 96383 Phocoenoides dalli M 214 A Phocoenidae
LACM 96487 Phocoenoides dalli M 210 A Phocoenidae
LACM 97203 Delphinus capensis M 219 A Delphinidae
LACM 97204 Delphinus capensis M 224 A Delphinidae
LACM 97207 Phocoenoides dalli M 210 A Phocoenidae
LACM 97284 Phocoenoides dalli M 217 A Phocoenidae
LACM 97405 Tursiops truncatus F 277 A Delphinidae
LACM 97429 Delphinus capensis M 232 A Delphinidae
LACM 97478 Delphinus capensis M 212 A Delphinidae
LACM 97489 Tursiops truncatus F 298 A Delphinidae
LACM 97490 Grampus griseus M 282 J Delphinidae
LACM 97491 Delphinus capensis M 219 A Delphinidae
LACM 97501 Mesoplodon perrini F 425 A Ziphiidae
LACM 97503 Delphinus capensis M 226 A Delphinidae
LACM 97504 Delphinus capensis M n/a U Delphinidae
LACM 97505 Tursiops truncatus F 267 J Delphinidae
LACM 97512 Delphinus capensis F 196 J Delphinidae
LACM 97513 Delphinus capensis F 195 J Delphinidae
LACM bowhead_a Balaena mysticetus U U U Balaenidae
LACM bowhead_b Balaena mysticetus U U U Balaenidae
LACM bowhead_c Balaena mysticetus U U U Balaenidae
224

Catalog Number Species Sex
Body
Length
Age Family
LACM bowhead_d Balaena mysticetus U U U Balaenidae
LACM bowhead_e Balaena mysticetus U U U Balaenidae
MAL 03-282 Balaenoptera
acutorostrata
F 730 A Balaenopteridae
MH 02-673 Physeter macrocephalus M 1400 J Physeteridae
MH 03-478 Balaenoptera physalus M 1600 J Balaenopteridae
MH 03-602 Megaptera novaeangliae M 1100 J Balaenopteridae
MH 03-616 Globicephala melas F 400 J Delphinidae
MH 03-621 Balaenoptera
acutorostrata
M 700 A Balaenopteridae
MJM 070110 Eubalaena glacialis M 1370 A Balaenidae
UMA 4820 Balaenoptera physalus F 2075 A Balaenopteridae
UMA 4920 Eubalaena glacialis F 1370 A Balaenidae
USNM 217912 Phocoena phocoena M U U Phocoenidae
USNM 22304 Tursiops truncatus U U U Delphinidae
USNM 239273 Tursiops truncatus F U U Delphinidae
USNM 252126 Tursiops truncatus U U U Delphinidae
USNM 258642 Tursiops aduncus M 287 A Delphinidae
USNM 395277 Stenella attenuata F 175 A Delphinidae
USNM 395390 Stenella attenuata M 218 A Delphinidae
USNM 395465 Stenella attenuata M 200 A Delphinidae
USNM 395599 Stenella longirostris M 173 A Delphinidae
USNM 396165 Tursiops truncatus M 303 A Delphinidae
USNM 396166 Inia geoffrensis F U U Iniidae
USNM 396304 Phocoenoides dalli M 202 A Phocoenidae
USNM 484929 Lissodelphis borealis M 265 A Delphinidae
USNM 484992 Tursiops truncatus M 239 J Delphinidae
USNM 500118 Tursiops aduncus F 239 J Delphinidae
USNM 500260 Delphinus delphis F 183 J Delphinidae
USNM 500261 Delphinus delphis M 186 J Delphinidae
USNM 500265 Delphinus delphis F 169 J Delphinidae
USNM 500268 Delphinus delphis F 185 J Delphinidae
USNM 500272 Delphinus delphis M 193 J Delphinidae
USNM 501148 Pontoporia blainvillei M 118 J Pontoporidae
USNM 501157 Pontoporia blainvillei F 136 A Pontoporidae
USNM 501172 Pontoporia blainvillei M 137 A Pontoporidae
USNM 501176 Pontoporia blainvillei F 142 A Pontoporidae
USNM 501179 Pontoporia blainvillei M 142 A Pontoporidae
USNM 501183 Pontoporia blainvillei F 145 A Pontoporidae
225

Catalog Number Species Sex
Body
Length
Age Family
USNM 501186 Pontoporia blainvillei F 143 A Pontoporidae
USNM 504107 Delphinus delphis M 209 A Delphinidae
USNM 504126 Grampus griseus M 298 A Delphinidae
USNM 504128 Mesoplodon carlhubbsi F 532 A Ziphiidae
USNM 504154 Lagenorhynchus acutus F 235 A Delphinidae
USNM 504279 Delphinus delphis U U U Delphinidae
USNM 504283 Delphinus delphis M 188 J Delphinidae
USNM 504302 Phocoena phocoena F 165 A Phocoenidae
USNM 504326 Tursiops truncatus F 203 J Delphinidae
USNM 504350 Stenella coeruleoalba M 231 A Delphinidae
USNM 504467 Steno bredanensis M 235 A Delphinidae
USNM 504468 Steno bredanensis M 227 A Delphinidae
USNM 504494 Steno bredanensis M 233 A Delphinidae
USNM 504530 Phocoena phocoena U U U Phocoenidae
USNM 504726 Tursiops truncatus M 298 A Delphinidae
USNM 504739 Tursiops truncatus M 250 J Delphinidae
USNM 504758 Stenella frontalis M 201 A Delphinidae
USNM 504773 Stenella coeruleoalba M 222 A Delphinidae
USNM 504879 Tursiops truncatus M 284 A Delphinidae
USNM 504919 Feresa attenuata U U U Delphinidae
USNM 504920 Pontoporia blainvillei F 155 A Pontoporidae
USNM 550042 Phocoena phocoena U 149 A Phocoenidae
USNM 550108 Grampus griseus F 277 J Delphinidae
USNM 550221 Steno bredanensis F 215 J Delphinidae
USNM 550312 Phocoena phocoena F 158 A Phocoenidae
USNM 550389 Feresa attenuata M 212 A Delphinidae
USNM 550391 Grampus griseus M 286 A Delphinidae
USNM 550393 Grampus griseus M 269 J Delphinidae
USNM 550401 Tursiops truncatus M 268 A Delphinidae
USNM 550422 Tursiops truncatus M 279 A Delphinidae
USNM 550432 Tursiops truncatus F 239 J Delphinidae
USNM 550436 Tursiops truncatus F 243 J Delphinidae
USNM 550440 Tursiops truncatus F 264 J Delphinidae
USNM 550495 Stenella coeruleoalba U U U Delphinidae
USNM 550496 Phocoena phocoena F 143 J Phocoenidae
USNM 550772 Tursiops truncatus F 270 J Delphinidae
USNM 550837 Steno bredanensis M 228 A Delphinidae
USNM 550852 Tursiops truncatus M 248 J Delphinidae
USNM 550877 Tursiops truncatus F 248 J Delphinidae
226

Catalog Number Species Sex
Body
Length
Age Family
USNM 550919 Tursiops truncatus F 283 A Delphinidae
USNM 550948 Tursiops truncatus F U U Delphinidae
USNM 550965 Stenella longirostris F 126 J Delphinidae
USNM 550969 Tursiops truncatus M 226 J Delphinidae
USNM 550995 Lagenorhynchus acutus M 253 A Delphinidae
USNM 571051 Tursiops truncatus M 277 A Delphinidae
USNM 571086 Tursiops truncatus M 273 A Delphinidae
USNM 571268 Feresa attenuata M 230 A Delphinidae
USNM 571327 Lagenorhynchus acutus M 253 A Delphinidae
USNM 571388 Tursiops truncatus F 285 A Delphinidae
USNM 571390 Lagenorhynchus acutus M 242 A Delphinidae
USNM 571521 Tursiops truncatus M 271 A Delphinidae
USNM 571709 Phocoena phocoena M 160 A Phocoenidae
USNM 571723 Phocoena phocoena M 146 A Phocoenidae
USNM 571725 Phocoena phocoena M 133 J Phocoenidae
USNM 571897 Tursiops truncatus F 240 J Delphinidae
USNM 571936 Tursiops truncatus F 276 J Delphinidae
USNM 572090 Tursiops truncatus F U U Delphinidae
USNM 572572 Tursiops truncatus F 103 J Delphinidae
USNM 572629 Phocoena phocoena F 163 A Phocoenidae
USNM 572632 Delphinus delphis M 223 A Delphinidae
USNM 572775 Delphinus delphis M 203 A Delphinidae
USNM 572776 Delphinus delphis M 228 A Delphinidae
USNM 572777 Delphinus delphis M 216 A Delphinidae
USNM 572784 Phocoena phocoena M 128 J Phocoenidae
USNM 572785 Phocoena phocoena M 152 A Phocoenidae
USNM 572828 Tursiops truncatus M 260 J Delphinidae
USNM 572859 Delphinus delphis F 207 A Delphinidae
USNM 572861 Phocoena phocoena U U U Phocoenidae
USNM 572871 Delphinus delphis M 229 A Delphinidae
USNM 572900 Delphinus delphis M 197 J Delphinidae
USNM 572949 Tursiops truncatus M 265 A Delphinidae
USNM 572980 Delphinus delphis M 225 A Delphinidae
USNM 593406 Tursiops truncatus M 279 A Delphinidae
USNM A20971 Ziphius cavirostris F 589 A Ziphiidae
USNM A49599 Ziphius cavirostris M 564 A Ziphiidae
UWBM 35430 Eschrichtius robustus M 1293 A Eschrichtiidae
UWBM 42003 Eschrichtius robustus M U U Eschrichtiidae
UWBM 42004 Balaenoptera musculus M 1830 J Balaenopteridae
227

Catalog Number Species Sex
Body
Length
Age Family
UWBM 42007 Eschrichtius robustus M 780 J Eschrichtiidae
UWBM 81848 Balaenoptera edeni M 1050 J Balaenopteridae
VMZ 2736 Balaenoptera physalus U U U Balaenopteridae
VMZ 2777 Balaenoptera musculus U U U Balaenopteridae
VMZ 2799 Eschrichtius robustus U U U Eschrichtiidae
VMZ Orca Orcinus orca U U U Delphinidae
VMZ Physeter Physeter macrocephalus U U U Physeteridae

Asset Metadata

Creator Dines, James P. (author)

Core Title The evolution and functional significance of the cetacean pelvic bones

Contributor Electronically uploaded by the author (provenance)

School College of Letters, Arts and Sciences

Degree Doctor of Philosophy

Degree Program Integrative and Evolutionary Biology

Publication Date 08/22/2016

Defense Date 06/17/2014

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag cetaceans,geometric morphometrics,mating systems,OAI-PMH Harvest,pelvic bones,sexual selection,testes evolution

Format application/pdf (imt)

Language English

Advisor McNitt-Gray, Jill L. (committee chair), Wang, Xiaoming (committee chair), Chuong, Cheng-Ming (committee member), Dean, Matthew D. (committee member)

Creator Email dines@usc.edu,jdines@nhm.org

Permanent Link (DOI) https://doi.org/10.25549/usctheses-c3-463453

Unique identifier UC11286789

Identifier etd-DinesJames-2840.pdf (filename),usctheses-c3-463453 (legacy record id)

Legacy Identifier etd-DinesJames-2840.pdf

Dmrecord 463453

Document Type Dissertation

Format application/pdf (imt)

Rights Dines, James P.

Type texts

Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Access Conditions The author retains rights to his/her dissertation, thesis or other graduate work according to U.S. copyright law. Electronic access is being provided by the USC Libraries in agreement with the a...

Repository Name University of Southern California Digital Library

Repository Location USC Digital Library, University of Southern California, University Park Campus MC 2810, 3434 South Grand Avenue, 2nd Floor, Los Angeles, California 90089-2810, USA

Abstract (if available)

Abstract Modern whales and dolphins evolved from four‐legged terrestrial mammals known from fossils that are 54 million years old. The gradual transition from living entirely on land to a fully aquatic existence in cetaceans was accompanied by a mosaic of adaptations for efficient locomotion in the marine environment. Among those adaptations are the progressive loss of external hindlimbs and the reduction of the pelvic girdle to a pair of unconnected pelvic bones. The remnant pelvic bones in cetaceans are often cited as useless vestigial structures, having no function but providing a glimpse of their evolutionary history. However, the pelvic bones in cetaceans, as in other tetrapods, are anchors for the genitalia and associated muscles. Cetacean pelvic bones also exhibit remarkable variation in shape and size among species, a pattern predicted by sexual selection theory. Sexual selection has been shown to influence the variation in the morphology of genitals and other structures related to mating in groups spanning invertebrates and vertebrates. The hypothesis that cetacean pelvic bones evolve in response to sexual selection is tested herein. ❧ The evolutionary history of cetaceans was reviewed, with special emphasis on tracing the progressive loss of the hind limb elements and reduction of the pelvic girdle. Using museum collections, more than 250 specimens representing 38 species were examined. Dissections on dead‐stranded cetacean carcasses provided new insights into pelvic bone orientation and muscle attachments within the organisms. Among the challenges in performing a quantitative analysis was the lack of identifiable landmarks in cetacean pelvic bones, which was resolved using three‐dimensional imaging technology and novel methods in geometric morphometrics. ❧ Since mating ecology is essentially unknown in most cetacean species, the variation in the relative size of testes among cetaceans was investigated. Relative testes size is a common proxy of mating system across diverse taxa with internal fertilization and is validated for cetaceans herein. For example, sperm competition theory predicts that species with promiscuous mating systems will have large relative testes. Similarly, there is expected to be a trade‐off between investment in weapons used in pre‐copulatory dominance contests and investment in testes mass. Both patterns hold true for cetaceans. As predicted, the patterns of variation in cetacean pelvic bones are correlated with variation in mating ecology, as inferred from relative testes mass. ❧ Cetaceans comprise a charismatic group of mammals that are an exemplar of natural selection. A rich fossil record documents their transition from quadrupedal land‐dwelling species to the fully aquatic modern forms with streamlined bodies. Among the dramatic morphologic changes in the evolutionary history of whales was the progressive loss of hindlimbs and reduction in the pelvic girdle, a trend that culminated in a pair of greatly reduced pelvic bones in modern species. Contrary to textbook descriptions, pelvic bones in modern cetaceans are not useless vestiges. Rather, cetacean pelvic bones play an essential role in mating ecology and reproductive fitness. In addition to pointing out the need to re‐write textbooks on evolution, this study is the first demonstration of sexual selection influencing internal reproductive structures.