Cetacean Evolution: Copulatory and Birthing Consequences of Pelvic and Hindlimb Reduction

Abstract

The earliest fossil cetaceans (archaeocetes) dramatically shifted the shape and articulation of the pelvis and hindlimbs during the land-to-sea transition. Archaeocetes were mostly semi-aquatic “walking whales” that used powerful hindlimbs to walk on land and swim to reach new aquatic sources of food. However, skeletons of the latest diverging lineages of archaeocetes, the basilosaurids, showed that the pelvis initially lost articulation with the sacrum, and hindlimbs were reduced and encased within the body wall. Consequently, basilosaurids were no longer able to bear their weight on land and probably had a different mating strategy compared to the other archaeocetes. Basilosaurid mating behaviors were probably consistent with those of modern cetaceans, including lateral- and ventral-facing copulation. Moreover, a pelvic girdle that was no longer constrained by vertebral and limb attachments likely freed fetal development from size constraints at birth, allowing for the birth of large fetuses. This study reports new data showing growth of the pelvis with age in modern bowhead whales (Balaena mysticetus) and their implications for left-right asymmetry and sex difference in pelvic dimensions among modern cetaceans. Reproductive structures present in modern cetaceans and artiodactyls were probably present in archaeocetes, including pelvic attachment of muscles associated with erection and mobility of the penis, the ischiocavernosus, in males and the clitoris of females. Within females, transverse folds along the vaginal canal are present in some terrestrial artiodactyls, modern cetaceans, and probably archaeocetes. Vaginal folds were probably exapted to assist in successful aquatic copulation in all fossil and modern cetaceans as they may protect some sperm from the lethal effects of sea water. Taken together, shifts in the pelvic girdle of cetaceans occurred over 40 million years ago and probably required changes in mating behaviors that were consistent with those seen in modern cetaceans.