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Nat Commun
2022 Nov 17;131:7039. doi: 10.1038/s41467-022-34474-4.
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The evolution of reproductive modes and life cycles in amphibians.
Liedtke HC
,
Wiens JJ
,
Gomez-Mestre I
.
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Amphibians have undergone important evolutionary transitions in reproductive modes and life-cycles. We compare large-scale macroevolutionary patterns in these transitions across the three major amphibian clades: frogs, salamanders, and caecilians. We analyse matching reproductive and phylogenetic data for 4025 species. We find that having aquatic larvae is ancestral for all three groups and is retained by many extant species (33-44%). The most frequent transitions in each group are to relatively uncommon states: live-bearing in caecilians, paedomorphosis in salamanders, and semi-terrestriality in frogs. All three groups show transitions to more terrestrial reproductive modes, but only in caecilians have these evolved sequentially from most-to-least aquatic. Diversification rates are largely independent of reproductive modes. However, in salamanders direct development accelerates diversification whereas paedomorphosis decreases it. Overall, we find a widespread retention of ancestral modes, decoupling of trait transition rates from patterns of species richness, and the general independence of reproductive modes and diversification.
Fig. 1: Phylogenetic distribution of reproductive modes in amphibians.
Species richness per amphibian group (top bar chart where Anura: dark blue gray, Caudata: mint green, Gymnophiona: lilac, and 1k = 1000 species) and frequencies of reproductive modes per group (percentages as pie charts), and per family (numbers of species as stacked bars on phylogeny). Reproductive modes are represented as blue = aquatic; dark green = semi-terrestrial; brown = terrestrial; light green = direct development; red = live-bearing; yellow = paedomorphism. Frequencies and percentages of unknown reproductive modes are depicted in light gray. The phylogeny shows the relationships of all 75 amphibian families, with icons and branch colors highlighting the three different amphibian clades. Source data are provided as a Source Data file.
Fig. 2: Schematics of four scenarios of reproductive-mode evolution.
Null: transitions between all states (reproductive modes) can occur. Non-sequential: derived (more terrestrial) states can only transition to and from the ancestral aquatic mode. Sequential: transitions can only occur between the ecologically most similar states. Semi-sequential: derived, fully terrestrial modes (direct development, live bearing and fully terrestrial biphasic) can only transition to and from the semi-terrestrial mode. Up to three variations of this final scenario were tested (dashed lines), allowing live-bearing to transition either to and from the aquatic mode, the semi-terrestrial mode, or direct development. Node colors and annotations reflect reproductive modes, where A, blue = aquatic; S, dark green = semi-terrestrial; T, brown = terrestrial; D, light green = direct development; L red = live-bearing; P, yellow = paedomorphism. Network edge colors and icons distinguish the three amphibian groups, where Anura: dark blue-gray, Caudata: mint green, Gymnophiona: lilac. Because not all six states are present in all three major clades of amphibians (nodes in gray), the scenarios vary between them.
Fig. 3: Estimated rates, frequencies and posterior sampling of reproductive-mode transitions in each major amphibian group.
a Estimated transition rates (×10−2) from best-performing corHMM models. Gray arrows and annotations represent hidden state rates. Rates lower than 0.01 are not shown. The best models for Anura and Caudata allowed for all rates to be different (except for pairs of rates annotated with an asterisk that have been forced to be symmetrical; see Methods), and the model for Gymnophiona had all rates set to be equal. b Numbers of transitions when estimating ancestral states at nodes only using joint estimations [Node-to-Node] and the mean numbers of transitions along branches [Anagenetic], estimated from 1000 stochastic character maps. Dashed lines indicate transitions only recovered using one of the two methods. The number of species per reproductive mode represented in the phylogeny are indicated in the nodes of the networks. c Proportions of models in the posterior where a given transition was estimated (i.e., non-zero transition rate) by the reverse jump MCMC of the MultiState Covarion algorithm implemented in BayesTraits. Proportions of 1 indicate transitions that were present in all models sampled by the MCMC. Transitions with proportions <0.5 are not shown. In all cases, color, position and letters of nodes are consistent and represent A, blue = aquatic; S, dark green = semi-terrestrial; T, brown = terrestrial; D, light green = direct development; L red = live-bearing; P, yellow = paedomorphism. Arrow weight is roughly proportional to transition rates (not to scale). Icons for each panel row distinguish the three amphibian groups. Source data are provided as a Source Data file.
Fig. 4: Net diversification rates (speciation minus extinction) per reproductive modes for Anura, Caudata and Gymnophiona.
a Distributions (with standard deviation error bars around the mean) of rates estimated per species in the phylogeny for each life-cycle category (i.e., tip rates). Species are categorized into biphasic life cycles (dark magenta), direct development (dark blue) or paedomorphism (yellow). Sample sizes (where n = number of species) for each are Anura: biphasic = 2608, direct development = 755; Caudata: biphasic = 192, direct development = 320, paedomorphism = 34; Gymnophiona: biphasic = 19, direct development = 43. Estimates were calculated using the best-fitting hisse models, which for Anura was a Reproductive mode Independent Diversification rate model (RmID) with hidden states, for Caudata was a Reproductive mode dependent Diversification rate model (RmDD) with hidden states, and for Gymnophiona was a Constant Diversification rate model (CD). In cases where models contained hidden states, rates are weighted averages per species. b Diversification rate estimates for each of the six reproductive modes, where blue = aquatic; dark green = semi-terrestrial; brown = terrestrial; light green = direct development; red = live-bearing; yellow = paedomorphism. Estimates are calculated using the best-fitting secsse models, which for Anura was a Reproductive mode Independent Diversification rate model (RmID) with hidden states, for Caudata was a Reproductive mode dependent Diversification model (RmDD) with hidden states, and for Gymnophiona was a Constant Diversification rate model (CD). In cases where models contained hidden states, rates shown are averaged across hidden and observed states. Icons in both panels distinguish the three amphibian groups. Source data are provided as a Source Data file.
