Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous–Paleogene boundary

Abstract

Frogs (Anura) are one of the most diverse groups of vertebrates and comprise nearly 90% of living amphibian species. Their worldwide distribution and diverse biology make them well-suited for assessing fundamental questions in evolution, ecology, and conservation. However, despite their scientific importance, the evolutionary history and tempo of frog diversification remain poorly understood. By using a molecular dataset of unprecedented size, including 88-kb characters from 95 nuclear genes of 156 frog species, in conjunction with 20 fossil-based calibrations, our analyses result in the most strongly supported phylogeny of all major frog lineages and provide a timescale of frog evolution that suggests much younger divergence times than suggested by earlier studies. Unexpectedly, our divergence-time analyses show that three species-rich clades (Hyloidea, Microhylidae, and Natatanura), which together comprise ∼88% of extant anuran species, simultaneously underwent rapid diversification at the Cretaceous-Paleogene (K-Pg) boundary (KPB). Moreover, anuran families and subfamilies containing arboreal species originated near or after the KPB. These results suggest that the K-Pg mass extinction may have triggered explosive radiations of frogs by creating new ecological opportunities. This phylogeny also reveals relationships such as Microhylidae being sister to all other ranoid frogs and African continental lineages of Natatanura forming a clade that is sister to a clade of Eurasian, Indian, Melanesian, and Malagasy lineages. Biogeographical analyses suggest that the ancestral area of modern frogs was Africa, and their current distribution is largely associated with the breakup of Pangaea and subsequent Gondwanan fragmentation. amphibia | Anura | nuclear genes | phylogeny | divergence time

Diversification of African tree frogs (genus Leptopelis) in the highlands of Ethiopia

“…Our divergence time estimates suggest that the genus Leptopelis diverged from other members of the family Arthroleptidae ~50 million years ago, similar to the ages reported by Portik and Blackburn () and Feng et al. (), as would be expected, as many of the samples and calibration points were obtained from those studies. The split between the Ethiopian Leptopelis and the rest of the genus (excluding L. parkeri ) occurred during the Miocene, ~16 mya, followed by the split of the arboreal forms ( L. ragazzii, L. vannutellii and L. yaldeni ) from L. gramineus + L. susanae , ~8 mya (Figure ).…”

The contribution of temperature and continental fragmentation to amphibian diversification

“…Another example involves a vicariance within Salamandridae (Pleurodelinae) between Nearctic and Palaearctic lineages in the early Eocene (Figure ). Our results are consistent with previous studies on amphibians proposing that the divergences of the main amphibian and anuran lineages may be related to vicariance events (Feng et al., ; Frazão et al., ; Pyron, ). The biogeographical analyses further suggest that vicariance was frequent and widespread across the amphibian phylogeny when the continental fragmentation increased during the Jurassic and throughout the Cretaceous (Figure ), and the frequency of these events tends to decrease after continental fragmentation slowed down in the Cenozoic (Appendix S9).…”

“…To address this question, amphibians (frogs, salamanders and caecilians) are a relevant clade because their relatively long evolutionary history ( ca . 300–270 Ma; Feller & Hedges, ; Feng et al., ; Pyron, ) has allowed long‐term fluctuations of temperature and number of landmasses to possibly affect their diversification. Indeed, amphibians have likely experienced the effect of continental fragmentation through time with the successive break‐up of Pangaea, Gondwana and Laurasia (San Mauro, Vences, Alcobendas, Zardoya, & Meyer, ).…”

Phylogeny of spiny frogs Nanorana (Anura: Dicroglossidae) supports a Tibetan origin of a Himalayan species group

“…Three carefully chosen fossil calibrations were selected to obtain divergence dates on the species tree and applied using an offset lognormal distribution: i) a minimum age of 33.9 Ma for the most recent common ancestor (MRCA) of Ranoidea based on the fossil Thaumastosaurus gezei (Rage & Roček, ), soft maximum 148.0 Ma (Feng et al, ) (95% CI: 34.5–148.0); ii) a minimum age of 25 for the MRCA of Ptychadena and Phrynobatrachus based on the earliest Ptychadenidae fossil (Blackburn, Roberts, & Stevens, ), soft maximum 148.0 Ma (Feng et al, ) (95% CI: 25.0–148.0); and iii) a minimum age of 15.97 Ma for the divergence of Hyla cinereus (North America) versus. Hyla annectans (Eurasia) based on the oldest fossils in Europe (Rage & Roček, ) (95% CI: 16.1–32.7; Roelants, Haas, & Bossuyt, ).…”