Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia

Abstract

Anolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis. This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification.

A highly conserved ontogenetic limb allometry and its evolutionary significance in the adaptive radiation of Anolis lizards

“…grass-bush, twig and crown-giant [ 65 , 66 ]), this adaptive radiation does not appear to involve profound changes to the underlying generative processes. Instead, the morphological variability of the Anolis limb seems perfectly capable of exploiting ecological opportunities, and the absence of certain morphologies from the mainland is better explained by ecological factors than by developmental innovations on islands [ 13 , 67 ]. This is consistent with a macroevolutionary perspective that suggests that drastic modifications of limb proportions are rare.…”

“…Measurements of adult limb elements were obtained from micro-CT scanning of museum specimens that were published elsewhere [ 12 , 13 ]. In brief, specimens were scanned using a GE phoenix v|tome|x m system (source voltage 100 kV; source current 200 µA; isometric voxel size 55–75 µm) at the Nanoscale Facility of the University of Florida, US.…”

“…Evolutionary allometric vectors (pPC1) were derived from phylogenetic PCAs in the R package ‘phytools’ [ 36 ] for each of the three major groups based on species means of each measurement and the phylogenetic tree published by Poe et al [ 26 ] with modifications described in [ 13 ]. We first assessed how well the phylogenetic allometric vectors of the three major groups are aligned with each other.…”

“…While an increasing number of studies compares trait covariation across species (e.g. [1,[11][12][13][14]), and sometimes relate these to ontogenetic trajectories [6,15,16], little has been done in the context of adaptive radiations. Thus, the extent to which ontogenetic covariation of morphological characters evolves, as well as the extent to which it contributes to the pattern of morphological diversification across the phylogeny, remains poorly understood.…”

Plant growth forms dictate adaptations to the local climate

“…Adaptive radiations are the source of much of the biodiversity on Earth, resulting from the evolution of phenotypic diversity in response to ecological shifts within a rapidly multiplying lineage ( Grant, 1981 ; Schluter, 2000 ; Givnish, 2015 ). Examples such as the Darwin finches from the Galapagos Islands, the Anolis lizards of the Greater Antilles and the cichlid fishes from East African lakes demonstrate how adaptations to the local environment result in a rapid accumulation of morphological and ecological diversity ( Grant, 1981 ; Losos et al., 1998 ; Schluter, 2000 ; Emerson, 2002 ; Grant and Grant, 2008 ; Losos and Ricklefs, 2009 ; Feiner et al., 2021 ; Ronco et al., 2021 ).…”