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. 2014 Nov;68(11):3296-306.
doi: 10.1111/evo.12516. Epub 2014 Oct 20.

Sexual selection targets cetacean pelvic bones

James P Dines  1 , Erik Otárola-Castillo, Peter Ralph, Jesse Alas, Timothy Daley, Andrew D Smith, Matthew D Dean
Affiliations

Sexual selection targets cetacean pelvic bones

James P Dines et al. Evolution. 2014 Nov.

Abstract

Male genitalia evolve rapidly, probably as a result of sexual selection. Whether this pattern extends to the internal infrastructure that influences genital movements remains unknown. Cetaceans (whales and dolphins) offer a unique opportunity to test this hypothesis: since evolving from land-dwelling ancestors, they lost external hind limbs and evolved a highly reduced pelvis that seems to serve no other function except to anchor muscles that maneuver the penis. Here, we create a novel morphometric pipeline to analyze the size and shape evolution of pelvic bones from 130 individuals (29 species) in the context of inferred mating system. We present two main findings: (1) males from species with relatively intense sexual selection (inferred by relative testes size) tend to evolve larger penises and pelvic bones compared to their body length, and (2) pelvic bone shape has diverged more in species pairs that have diverged in inferred mating system. Neither pattern was observed in the anterior-most pair of vertebral ribs, which served as a negative control. This study provides evidence that sexual selection can affect internal anatomy that controls male genitalia. These important functions may explain why cetacean pelvic bones have not been lost through evolutionary time.

Keywords: Morphological evolution; sexual conflict; sexual selection.

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Figures

Figure 1
Figure 1
Skeletal anatomy of the bottlenose dolphin (Tursiops truncatus). (A) External hindlimbs have been lost, and the pelvic girdle is reduced to a pair of small bones that no longer articulates with the skeleton. An adult male of approximately 3 meters. Artwork: Carl Buell. Used with permission from John Gatesy. (B) A closeup of the pelvic bone (cream colored), showing the soft tissue anatomy (pink). Labels indicate one of the paired ischiocavernosus muscles, the retractor penis muscle (Retractor) that holds the penis inside the body, and the genital slit of a male dolphin. Despite recent reports, the retractor penis muscle does not attach to the pelvic bone, and its sole function appears to be for holding the penis inside the body (Ommanney 1932); a male erection is therefore accompanied by relaxation of the retractor penis muscle, allowing the penis to extend outside the body. (C) Laser scans from paired pelvic bones (dorsal view, anterior towards top of figure) with 962 semi-landmarks (green) (see Figures S3–S4 for more detail). These pelvic bones are approximately 11 cm long. (D) Laser scans and semi-landmarks from the anterior-most pair of ribs. These rib bones are approximately 14 cm long.
Figure 2
Figure 2
Phylogeny of cetacean taxa (McGowen et al. 2009) with known maximum testes size and body length. Numbers to the left of parentheses indicate residual testes mass (calculated as in Fig. S1). Numbers in parentheses indicate the number of individuals sampled for male pelvic, male rib, female pelvic, and female rib bones, respectively. Images indicate representative body morphology (left column, artwork from Carl Buell, used with permission from John Gatesy), paired pelvic bones (middle column), and paired rib bones (right column) from a subset of species. N/A=rib bones could not be sampled from all museum specimens.
Figure 3
Figure 3
Among sexually mature males, residual centroid size (species-average centroid size regressed onto body length) was positively correlated with residual testes mass (using PGLS methodology) in (A) pelvic bones, but not (B) ribs. Species: 1-Balaenoptera acutorostrata, 2-Balaenoptera musculus, 3-Delphinus capensis, 4-Delphinus delphis, 5-Eschrichtius robustus, 6-Eubalaena glacialis, 7-Feresa attenuata, 8-Grampus griseus, 9-Inia geoffrensis, 10-Lagenorhynchus acutus, 11-Lagenorhynchus obliquidens, 12-Lissodelphis borealis, 13-Phocoena phocoena, 14-Phocoenoides dalli, 15-Pontoporia blainvillei, 16-Pseudorca crassidens, 17-Stenella attenuata, 18-Stenella coeruleoalba, 19-Stenella frontalis, 20-Stenella longirostris, 21-Steno bredanensis, 22-Tursiops truncatus, 23-Ziphius cavirostris.
Figure 4
Figure 4
The results of a customized Bayesian model of correlated evolution between traits. (A) All 1000 correlation coefficients sampled from the marginal posterior distributions showed that shifts in relative testes mass positively predicted shifts in pelvic centroid size (correlation rho=0.67, 95% credible interval: 0.25 to 0.90). (B) In contrast, shifts in testes size did not predict shifts in rib centroid size (correlation rho=0.05, 95% credible interval: −0.38 to 0.48).
Figure 5
Figure 5
(A) Among nine independent species pairs (filled circles each represent a species pair), pelvic bone shape divergence was positively correlated with divergence in testes residuals (p=0.008, r=0.81). (B) In contrast, rib shape divergence was not correlated with divergence in testes size residuals (p=0.72, r=−0.14). For completeness, the data for all pairwise contrasts, including non-independent contrasts, is shown in gray circles, although they were not included in tests of correlation. Only sexually mature males for which both pelvic and rib bones could be sampled were included; Species pairs: 1=Delphinus capensis vs. Delphinus 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, 9=Stenella coeruleoalba vs. Stenella frontalis.
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