Global patterns of diversification in the history of modern amphibians

Abstract

The fossil record of modern amphibians (frogs, salamanders, and caecilians) provides no evidence for major extinction or radiation episodes throughout most of the Mesozoic and early Tertiary. However, long-term gradual diversification is difficult to reconcile with the sensitivity of present-day amphibian faunas to rapid ecological changes and the incidence of similar environmental perturbations in the past that have been associated with high turnover rates in other land vertebrates. To provide a comprehensive overview of the history of amphibian diversification, we constructed a phylogenetic timetree based on a multigene data set of 3.75 kb for 171 species. Our analyses reveal several episodes of accelerated amphibian diversification, which do not fit models of gradual lineage accumulation. Global turning points in the phylogenetic and ecological diversification occurred after the end-Permian mass extinction and in the late Cretaceous. Fluctuations in amphibian diversification show strong temporal correlation with turnover rates in amniotes and the rise of angiosperm-dominated forests. Approximately 86% of modern frog species and >81% of salamander species descended from only five ancestral lineages that produced major radiations in the late Cretaceous and early Tertiary. This proportionally late accumulation of extant lineage diversity contrasts with the long evolutionary history of amphibians but is in line with the Tertiary increase in fossil abundance toward the present.

Fig. 1.

Phylogenetic patterns of net diversification in the history of modern amphibians. (a) Evolutionary timetree based on the ML tree, Thorne and Kishino's relaxed molecular clock model, and minimum time constraints on 22 amphibian divergences derived from fossil and paleogeographic evidence (see SI Text and SI Table 2). Divergence time estimates and corresponding 95% credibility intervals for all nodes are provided in SI Data Set 1. Branch support is indicated as follows: filled squares, ML bootstrap support ≥75% and Bayesian posterior probability ≥0.95; right-pointing filled triangles, bootstrap support <75% and Bayesian posterior probability ≥0.95; left-pointing filled triangles, bootstrap support ≥75% and Bayesian posterior probability <0.95. Label numbers represent rank positions when clades are sorted from highest net diversification rate to lowest. Divergences that represent at least a doubling of the clade-specific net diversification rate are indicated in bold. (b) Net diversification rates estimated per clade under relative extinction rates d:b = 0 (red) and d:b = 0.95 (blue). Clade numbers are cross-referenced in the timetree. (c) Comparison of the proportional diversity of extant clades at the beginning of the late Cretaceous and at present.

Fig. 2.

Global patterns of amphibian net diversification. (a) LTT plot derived from the timetree, compared with constant-diversification models with relative extinction rates (b:d) ranging from 0 to 0.95. Asterisks indicate rejection of the null model by a goodness-of-fit test and a Markov-chain constant-rate test (Bonferroni-corrected α = 0.01). (b) RTT plot showing net diversification rates estimated under d:b = 0 (red) and d:b = 0.95 (blue) for successive 20-Myr intervals (280–100 Mya) and 10-Myr intervals (100–20 Mya). Rate estimates that significantly differ from those expected under constant diversification along the entire plot (P < 0.05) are indicated by a circle (d:b = 0) or an asterisk (d:b = 0.95). (c) Comparison of amphibian net diversification rates (blue, back) with amniote family origination and extinction rates documented by the fossil record (green, middle and red, front, respectively) (4). Note that amphibian and amniote rates are represented at different scales. The green rectangle represents the time window in which angiosperms underwent their major radiation (47).