Abstract

Diversifications often proceed along highly conserved, evolutionary trajectories. These patterns of covariation arise in ontogeny, which raises the possibility that adaptive morphologies are biased towards trait covariations that resemble growth trajectories. Here, we test this prediction in the diverse clade of Anolis lizards by investigating the covariation of embryonic growth of 13 fore- and hindlimb bones in 15 species, and compare these to the evolutionary covariation of these limb bones across 267 Anolis species. Our results demonstrate that species differences in relative limb length are established already at hatching, and are resulting from both differential growth and differential sizes of cartilaginous anlagen. Multivariate analysis revealed that Antillean Anolis share a common ontogenetic allometry that is characterized by positive allometric growth of the long bones relative to metapodial and phalangeal bones. This major axis of ontogenetic allometry in limb bones deviated from the major axis of evolutionary allometry of the Antillean Anolis and the two clades of mainland Anolis lizards. These results demonstrate that the remarkable diversification of locomotor specialists in Anolis lizards are accessible through changes that are largely independent from ontogenetic growth trajectories, and therefore likely to be the result of modifications that manifest at the earliest stages of limb development.

Highlights

  • Morphological diversification of ecologically specialized forms is a hallmark of adaptive radiations

  • If the regulation of development and growth were to exercise a substantial effect on adaptive diversification, distantly related species should share similar patterns of morphological covariation in ontogeny, and this may force adult morphologies to diverge along the same dimensions

  • Eleven species of the embryonic dataset belong to the Greater Antillean group, three to the Northern Lesser Antillean group that is nested within the Greater Antillean group and one to the Southern Lesser Antillean group that diverged from the Primary Mainland group early in the evolutionary history of Anolis

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Summary

Introduction

Morphological diversification of ecologically specialized forms is a hallmark of adaptive radiations. The morphological differences that accrue are often substantial, but comparison of adult phenotypes reveals that even extreme cases of diversification tend to preserve covariation between characters [1,2,3]. One explanation for this is that the phenotypic variation that selection can act upon is highly structured by development [4]. If the regulation of development and growth were to exercise a substantial effect on adaptive diversification, distantly related species should share similar patterns of morphological covariation in ontogeny, and this may force adult morphologies to diverge along the same dimensions (i.e. developmental lines of least resistance [4,10]).

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