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. 2024 Jun 3;8(5):623-637.
doi: 10.1093/evlett/qrae022. eCollection 2024 Sep.

Opportunity begets opportunity to drive macroevolutionary dynamics of a diverse lizard radiation

Laura R V Alencar  1 , Orlando Schwery  2 , Meaghan R Gade  1 , Saúl F Domínguez-Guerrero  1 , Eliza Tarimo  2 , Brooke L Bodensteiner  1 , Josef C Uyeda  2 , Martha M Muñoz  1
Affiliations

Opportunity begets opportunity to drive macroevolutionary dynamics of a diverse lizard radiation

Laura R V Alencar et al. Evol Lett. .

Abstract

Evolution proceeds unevenly across the tree of life, with some lineages accumulating diversity more rapidly than others. Explaining this disparity is challenging as similar evolutionary triggers often do not result in analogous shifts across the tree, and similar shifts may reflect different evolutionary triggers. We used a combination of approaches to directly consider such context-dependency and untangle the complex network of processes that shape macroevolutionary dynamics, focusing on Pleurodonta, a diverse radiation of lizards. Our approach shows that some lineage-wide signatures are lost when conditioned on sublineages: while viviparity appears to accelerate diversification, its effect size is overestimated by its association with the Andean mountains. Conversely, some signals that erode at broader phylogenetic scales emerge at shallower ones. Mountains, in general, do not affect speciation rates; rather, the occurrence in the Andean mountains specifically promotes diversification. Likewise, the evolution of larger sizes catalyzes diversification rates, but only within certain ecological and geographical settings. We caution that conventional methods of fitting models to entire trees may mistakenly assign diversification heterogeneity to specific factors despite evidence against their plausibility. Our study takes a significant stride toward disentangling confounding factors and identifying plausible sources of ecological opportunities in the diversification of large evolutionary radiations.

Keywords: Andes; body size; diversification; reptiles; viviparity.

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Figures

Figure 1.
Figure 1.
Overview of the methodological framework used to disentangle the effects of ecological opportunities on the diversification of Pleurodonta lizards. Through this combination of approaches, users can isolate and quantify independent signals of ecological opportunity on diversification rates. Initially, we identify lineages exhibiting unique macroevolutionary signals (i.e., significant shifts in diversification rates) (Step 1). Subsequently, through examination of these lineages and their natural history, we test hypotheses potentially linking their biology with the identified macroevolutionary signals (Step 2). Given the association of multiple traits with diversification rates, we employ SSE approaches to untangle their relative effects on diversification rate heterogeneity. Using MiSSE, we first quantify the number and location of rate categories required to explain rate heterogeneity (Step 3A). We then use a customized MuSSE analysis to investigate the effect of each trait on diversification rates within the rate categories suggested by MiSSE (Step 3B). Finally, we conduct an additional MuSSE analysis in one of the suggested MiSSE regimes (i.e., Liolaemus) to disentangle the relative contributions of the two traits when considered together (Step 4). This combination of approaches resolves a false positive. Specifically, we observe that the evolution of viviparity appears to enhance species diversification, although its true impact is inflated by its association with the Andean mountains.
Figure 2.
Figure 2.
Tip-speciation rates widely vary across Pleurodonta lizards and have been likely shaped by the distinct sources of ecological opportunities encountered during their radiation. Dots indicate speciation rate shifts inferred by BAMM (Supplementary Figure S9). Images depict some Pleurodonta species from left to right and top to bottom: Anolis biporcatus by J. Salazar, Phrynosoma orbiculare by S. Domínguez-Guerrero, Amblyrhynchus cristatus by Reptiles of Ecuador Project, and Liolaemus gardeli by M. Borges-Martins.
Figure 3.
Figure 3.
Speciation rates are higher among viviparous species compared to oviparous ones. Higher speciation rates in viviparous species are associated with drier and more topographically complex environments. Speciation rates are also higher among species that occur in Andean mountains compared to those occurring in other regions, even when analyzing viviparous species only. See Supplementary Table S3 for parameter estimates from PGLS analyses.
Figure 4.
Figure 4.
Speciation rates per source of ecological opportunity. Triangles represent species that are viviparous, arboreal, and insular, occur on mountains or specifically in the Andean mountains, and are also evolving toward large body size optima as suggested by bayou analyses. Dashed lines represent the median speciation rates of species evolving toward large body size optima (upper line) and the median speciation rates of the remaining species (bottom line). See Supplementary material for how we define “large body size optima.”
Figure 5.
Figure 5.
Relative contributions of reproduction mode (oviparity or viviparity) and Andean mountains (presence or absence) in driving rate heterogeneity across Pleurodonta. Phylogenies show the four rate categories (i.e., Liolaemus, Phymaturus, iguanas + Sceloporus subclade, background) that best explain the diversification rate heterogeneity in Pleurodonta according to MiSSE analysis. Violin plots show the net diversification rates for species occurring in the Andean mountains or not and for oviparous or viviparous species within each of the rate categories detected by MiSSE. Letters represent the rate categories and numbers represent the states (e.g., on the left panels: 0A absence in the Andes, 1A presence in the Andes; on the right panels: 0A oviparous, 1A viviparous). Dark colors correspond to trait presence. Categories and states 1D (left panel) and 0C (right panel) represent the prior as there are no Andean or oviparous species within iguanas + Sceloporus subclade and Phymaturus, respectively.
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