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

Abstract

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.fitness tradeoff ͉ genital evolution ͉ mate choice ͉ natural selection ͉ sexual selection

Predictors of male insemination success in the mosquitofish (Gambusia holbrooki)

“…2010; G. affinis : Langerhans et al. 2005). However, gonopodium length might also reduce male maneuverability: Male G. affinis with longer gonopodia relative to their body size have slower burst swimming speed (Langerhans et al.…”

“…However, gonopodium length might also reduce male maneuverability: Male G. affinis with longer gonopodia relative to their body size have slower burst swimming speed (Langerhans et al. 2005). Here, we extend previous work by taking a multivariate approach to examining how male traits influence insemination success.…”

Females prefer to associate with males with longer intromittent organs in mosquitofish

“…Closely related poeciliids often vary greatly in relative gonopodium length (Rosen & Tucker 1961). A female preference for males with longer gonopodia has only been shown in one species (Gambusia affinis) using video playbacks (Langerhans et al 2005) and there is a weak correlative evidence for a similar preference in Poecilia reticulata (Brooks & Caithness 1995). To date, no study has actively manipulated the genital size of live fish.…”

“…In addition, population variation in male genitals is associated with changes in the use of different mating tactics and predation risk (e.g. Kelly et al 2000;Jennions & Kelly 2002;Langerhans et al 2005). Male poeciliids inseminate females with their gonopodium, an intromittent organ modified from the anal fin.…”

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification

“…Indeed, genital structures exhibit far greater levels of complexity than is thought necessary for simply transferring sperm to females, and there is now widespread evidence that sexual selection is responsible for such complexity [1,2]. Much of this evidence comes from studies linking variation in male genital morphology to either mating success [3][4][5][6] or paternity success [7][8][9][10][11], although further evidence comes from comparative studies revealing positive associations between the rate of divergent evolution of male genitalia and the intensity of sexual selection acting on these traits (e.g. [12]).…”