Male genital size reflects a tradeoff between attracting mates and avoiding predators in two live-bearing fish species

Male genitalia may experience more rapid, divergent evolution than any other animal character, but why? Research during the past several decades has culminated in the view that genital diversification primarily results from postmating sexual selection (e.g., sperm competition or cryptic female choice). However, the potential roles of premating sexual selection (e.g., mate choice) and natural selection have received little attention. We examined the possible importance of these mechanisms by investigating divergence in male genitalia among populations differing in predator regime for two species of live-bearing fish (Gambusia affinis in Texas and Gambusia hubbsi in The Bahamas). When controlled for body size, males exhibited a larger gonopodium (sperm-transfer organ) in predator-free environments than in predatory environments, a trend that persisted across space (multiple populations), time (multiple years), and species. By conducting laboratory experiments with G. affinis, we found that premating sexual selection seems to favor larger male genitalia (females exhibited mating preference for males having larger gonopodia), but natural selection in the presence of predatory fishes seems to favor reduced genital size (larger gonopodium size was associated with reduced burst-swimming performance, an important antipredator behavior). Although postmating sexual selection is widely presumed to be the most important mechanism driving genital diversification, these findings suggest that alternative mechanisms, particularly for organisms that cannot retract their genitalia, may also prove important.