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

Abstract

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.

Comparative Postembryonic Skeletal Ontogeny in Two Sister Lineages of Old World Tree Frogs (Rhacophoridae: Taruga, Polypedates)

“…The evolution of the spectacular diversity of reproductive modes in rhacophorids shows that both terrestrial direct-developing and foam-nesting species arise through gel-nesting ancestors, while basal rhacophorids are aquatic breeders [15]. The terrestrial direct-developing forms, which spend their entire embryonic sequence within eggs, are placed in three well-supported clades― Philautus , Pseudophilautus and Raorchestes .…”

“…Finally, foam-nesting genera are in two paraphyletic clades ( Rhacophorus , Polypedates , Taruga , Ghatixalus in one clade and Chiromantis as another). These have terrestrial foam nests and postembryonic free-swimming tadpoles [2,5,6,13,15]. Skeletal ontogeny across developmental stages of these forms is not known, except for a single study on Pseudophilautus silus [17].…”

Evidence for parental care in Feihyla kajau (Anura: Rhacophoridae)

“…Feihyla kajau (Dring, 1983), a Bornean endemic (Inger et al 2004), is the only representative of the exclusively Southeast Asian genus Feihyla found on the island (Hertwig et al 2013, AmphibiaWeb 2018. Like other rhacophorids with arboreal gel nests, F. kajau is relatively small and lays small egg clutches (Meegaskumbura et al 2015). To date, there is no available information on parental egg attendance in this species.…”

“…They reproduce by aquatic breeding, direct development, or laying eggs in foam nests or terrestrial "gel nests" (Meegaskumbura et al 2015). The basal state to direct development and foam nesting in rhacophorids may be gel-nesting, in which terrestrial eggs are sheathed in a thick jelly (Meegaskumbura et al 2015).…”

“…They reproduce by aquatic breeding, direct development, or laying eggs in foam nests or terrestrial "gel nests" (Meegaskumbura et al 2015). The basal state to direct development and foam nesting in rhacophorids may be gel-nesting, in which terrestrial eggs are sheathed in a thick jelly (Meegaskumbura et al 2015). Feihyla kajau (Dring, 1983), a Bornean endemic (Inger et al 2004), is the only representative of the exclusively Southeast Asian genus Feihyla found on the island (Hertwig et al 2013, AmphibiaWeb 2018.…”