Patterns of reproductive‐mode evolution in Old World tree frogs (Anura, Rhacophoridae)

Abstract

The Old World tree frogs (Anura: Rhacophoridae), with 387 species, display a remarkable diversity of reproductive modes – aquatic breeding, terrestrial gel nesting, terrestrial foam nesting and terrestrial direct development. The evolution of these modes has until now remained poorly studied in the context of recent phylogenies for the clade. Here, we use newly obtained DNA sequences from three nuclear and two mitochondrial gene fragments, together with previously published sequence data, to generate a well‐resolved phylogeny from which we determine major patterns of reproductive‐mode evolution. We show that basal rhacophorids have fully aquatic eggs and larvae. Bayesian ancestral‐state reconstructions suggest that terrestrial gel‐encapsulated eggs, with early stages of larval development completed within the egg outside of water, are an intermediate stage in the evolution of terrestrial direct development and foam nesting. The ancestral forms of almost all currently recognized genera (except the fully aquatic basal forms) have a high likelihood of being terrestrial gel nesters. Direct development and foam nesting each appear to have evolved at least twice within Rhacophoridae, suggesting that reproductive modes are labile and may arise multiple times independently. Evolution from a fully aquatic reproductive mode to more terrestrial modes (direct development and foam nesting) occurs through intermediate gel nesting ancestral forms. This suggests that gel nesting is not only a possible transitional state for the evolution of terrestriality, but also that it is a versatile reproductive mode that may give rise to other terrestrial reproductive modes. Evolution of foam nesting may have enabled rhacophorids to lay a larger number of eggs in more open and drier habitats, where protection from desiccation is important. Terrestrial direct development allows frogs to lay eggs independent of bodies of water, in a diversity of humid habitats, and may represent a key innovation that facilitated the evolution of nearly half of all known rhacophorid species.