Polyandry, Predation, and the Evolution of Frog Reproductive Modes

Abstract

Frog reproductive modes are complex phenotypes that include egg/clutch characteristics, oviposition site, larval development, and sometimes, parental care. Two evident patterns in the evolution of these traits are the higher diversity of reproductive modes in the tropics and the apparent progression from aquatic to terrestrial reproduction, often attributed to higher fitness resulting from decreased predation on terrestrial eggs and tadpoles. Here, we propose that sexual selection-and not only natural selection due to predation-favors terrestrial breeding by reducing the loss of fitness due to polyandry. To examine this novel selective mechanism, we reconstructed the evolution of reproductive diversity in two frog families (Hylidae and Leptodactylidae) and tested for concerted evolution of egg and tadpole development sites with specific mating behaviors. We found that oviposition and tadpole development sites are evolving independently, do not show the same diversity and/or directionality in terms of terrestriality, and thus may be diversifying due to different selective mechanisms. In both families, terrestrial egg deposition is correlated with amplexus that is hidden from competing males, and in hylids, testes mass was significantly larger and more variable in males with exposed amplexus that are vulnerable to polyandry. Our results indicate that intrasexual selection has been an underappreciated mechanism promoting diversification of frog reproductive modes.

Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation?

“…For example, the lowered risk of sperm loss and heightened sperm longevity and fertilization efficiency through foam nesting has been suggested to intensify sperm competition compared to strictly aquatic spawning (Byrne et al 2002). Further, a recent study suggests that the repeated evolutionary transition to terrestrial oviposition in hylid and leptodactylid frogs may be linked to a higher chance of hidden amplexus on land than in the water, thereby favoring males that can lower the risk of multi-male spawning through terrestrial mating (Zamudio et al 2016). It would thus be interesting to disentangle the links between different forms of polyandry (from multi-male amplexus to clutch piracy) and spawning conditions, including the relative timing of gamete release between the sexes, to better understand the fertilization processes and selection on different ejaculate traits.…”

Male‐male competition and repeated evolution of terrestrial breeding in Atlantic Coastal Forest frogs*

“…Our analyses indicate that predator avoidance may not be the only driver of the highly diverse reproductive modes observed in tropical frogs (Haddad and Prado ; Verdade ; Zamudio et al. ). Although avoidance of aquatic predators may be important in some cases, in lineages with high degrees of male‐male competition and high costs of territoriality, an equally important selective force may be avoidance of those costs.…”

“…An alternative hypothesis posits that terrestrial breeding decreases male‐male competition that is typical of high‐density aquatic breeding habitats (Zamudio et al. ). Terrestrial breeding reduces the need for costly behaviors associated with male defense of territories and females, and also reduces the potential for fitness loss due to polyandry that can occur in breeding aggregations where males directly compete for females (Zamudio et al.…”

“…Terrestrial breeding reduces the need for costly behaviors associated with male defense of territories and females, and also reduces the potential for fitness loss due to polyandry that can occur in breeding aggregations where males directly compete for females (Zamudio et al. ).…”

“…); and (3) males, but not females, decrease in size in terrestrial species because shifts to terrestriality impose lower sexual selection for large body sizes due to lower levels of male‐male competition (Zamudio et al. ), and this in turn results in larger SSD in terrestrial species.…”