Evolution of genitalia: theories, evidence, and new directions

Abstract

Many hypotheses have been proposed to explain why male intromittent genitalia consistently tend to diverge more rapidly than other body traits of the same individuals in a wide range of animal taxa. Currently the two most popular involve sexual selection: sexually antagonistic coevolution (SAC) and cryptic female choice (CFC). A review of the most extensive attempts to discriminate between these two hypotheses indicates that SAC is not likely to have played a major role in explaining this pattern of genital evolution. Promising lines for future, more direct tests of CFC include experimental modification of male genital form and female sensory abilities, analysis of possible male-female dialogues during copulation, and direct observations of genital behavior.

Experimental coevolution of male and female genital morphology

“…Future studies of female genital evolution and coevolution should focus on structures that interact directly with male genitalia, and on the sensory physiology of female genital tracts 7 . Although our data provide unequivocal evidence that sexual selection drives the correlated evolution of male and female genital morphology, distinguishing between the proposed mechanisms of sexual selection is difficult 11 . Sexual conflict in our sexually selected lines may have favoured the evolution of female morphology that makes it more difficult for males to gain genital coupling, which in turn may have favoured the evolution of an elongated aedeagus that allows a male to reach the female's genital pits at a direct cost to female fitness.…”

“…Critically, studies documenting the experimental evolution of male genital morphology have provided evidence that sexual selection underlies these macro-evolutionary patterns 3 . Cryptic female choice 2 and sexually antagonistic coevolution 10 represent two mechanisms for the evolution of genital morphology via sexual selection 11 . Cryptic female choice proposes that females bias paternity toward males whose genitalia are better able to deliver the appropriate fit and/or stimulation during copulation, and that this cryptic preference delivers indirect genetic benefits in the form of sons better equipped to gain fertilizations, and/or offspring that, on average, have a higher viability 12 .…”

Genetic and phenotypic influences on copulatory plug survival in mice

“…Sexual selection is thought to play a central role in driving the rapid evolution of animal reproductive traits (Andersson, 1994;Eberhard, 2009). Diverse aspects of ejaculate composition (volume, sperm count and abundance of accessory proteins) and biochemical function (coagulation and induction of female immune response) can evolve rapidly, especially in species where females mate with multiple males (Pilch and Mann, 2006;Poiani, 2006;Cameron et al, 2007;Robertson, 2007).…”

Deep homology in the age of next-generation sequencing

“…Intriguingly, a similar co-option of an ancestral gene regulatory network seems to have paved the way for the emergence of morphological novelties in the external genitalia of several members of the Drosophila melanogaster clade [59]. Although shared developmental trajectories seem unlikely in this case of regulatory co-option, the Drosophila example further underscores the power of reutilizing pre-existing genetic cassettes, especially in rapidly evolving structures such as external genitalia [60,61].…”