Habitat use affects morphological diversification in dragon lizards

Abstract

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock-dwelling, terrestriality, semi-arboreality and arboreality. Given these reconstructions, we fit models of evolution to species' morphological trait values and find that rock-dwelling and arboreality limit diversification relative to terrestriality and semi-arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model-averaged rate estimates are slowest for these habitat types. These results suggest that ground-dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.

Fig. 1

Maximum clade credibility phylogeny for 90 agamid species illustrating a single reconstruction of structural habitat use. Nodes are supported by > 0.95 Bayesian posterior probabilities unless otherwise noted, and branch lengths are proportional to time (i.e. root node depth is 1.0). Colour/shade of branches indicates inferred habitat use based on stochastic character mapping (see key). Habitat states for species are given by colour/shade of terminal nodes. Transitions between habitat states are highlighted by vertical, black bars. We used this reconstruction of phylogeny and habitat state and 499 others as the basis for fitting models of evolution in which rates of morphological diversification are allowed to differ in lineages that use different habitat types.

Fig. 2

Scatterplots of agamid species in a morphospace defined by principal components 2 and 3. Color-coding for species’ habitat states is the same as in Fig. 1. Loadings of original variables on PCs are described for each axis. For brevity, we use ‘hindlimb length’ and ‘forelimb length’ to describe loadings on PCs when more than one element of that limb loads strongly on that axis. See Table 2 for details about PCA.

Fig. 3

Model-averaged estimates for the rates of PC evolution in rock-dwelling (grey), arboreal (green), semi-arboreal (blue) and terrestrial (yellow) lineages. Point estimates are means of rate estimates from the 10 multiple-rate models and have been weighted by Akaike weights. Error bars are standard errors, representing uncertainty in habitat and phylogenetic reconstructions. Note that the y-axis for PC 1, an axis of size variation, is different from the y-axis for PCs 2, 3 and 4, which describe shape.

Fig. 4

Rates of size and shape evolution for each habitat category estimated within the major agamid clades. Point estimates for the rates of size evolution are means of estimates for the rates of PC 1 evolution across the 500 habitat reconstructions, and estimates for the rates of shape evolution are sums of the mean rate estimates for PCs 2, 3 and 4. Error bars are standard errors for the rate estimates across the 500 reconstructions. Shapes correspond to clade identity (see Fig. 1): diamonds are southwest Asian/African lineages, triangles are southeast Asian lineages, and squares are Australian lineages. Horizontal lines represent rate estimates for all Agamidae (based on the full, four-rate Brownian model), and grey boxes represent ± one standard error taken across reconstructions.