Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs

Carla Bardua,Julien Clavel,Anjali Goswami,Edward L Stanley,Kalpana Das,Anne-Claire Fabre,Margot Bon,David C Blackburn

doi:10.1038/s41467-021-22792-y

Abstract

Habitat is one of the most important factors shaping organismal morphology, but it may vary across life history stages. Ontogenetic shifts in ecology may introduce antagonistic selection that constrains adult phenotype, particularly with ecologically distinct developmental phases such as the free-living, feeding larval stage of many frogs (Lissamphibia: Anura). We test the relative influences of developmental and ecological factors on the diversification of adult skull morphology with a detailed analysis of 15 individual cranial regions across 173 anuran species, representing every extant family. Skull size, adult microhabitat, larval feeding, and ossification timing are all significant factors shaping aspects of cranial evolution in frogs, with late-ossifying elements showing the greatest disparity and fastest evolutionary rates. Size and microhabitat show the strongest effects on cranial shape, and we identify a “large size-wide skull” pattern of anuran, and possibly amphibian, evolutionary allometry. Fossorial and aquatic microhabitats occupy distinct regions of morphospace and display fast evolution and high disparity. Taxa with and without feeding larvae do not notably differ in cranial morphology. However, loss of an actively feeding larval stage is associated with higher evolutionary rates and disparity, suggesting that functional pressures experienced earlier in ontogeny significantly impact adult morphological evolution.

Highlights

Habitat is one of the most important factors shaping organismal morphology, but it may vary across life history stages
The presence of an actively feeding larval stage has been hypothesised to be an ontogenetic constraint on the adult morphology, whereas the loss of an actively feeding larval stage has been suggested to promote morphological novelty[19,20,41,42] and drive increased rates of morphological evolution[11,21,22]
If the anuran larval stage acts as a developmental module that fully decouples larval and adult phenotypic evolution, we would expect no differences in adult morphological evolution between taxa with different life history strategies

Summary

Introduction

Habitat is one of the most important factors shaping organismal morphology, but it may vary across life history stages. Taxa with feeding larvae require distinct functional adaptations for their larval and adult environments, given the distinct changes in feeding mechanisms across the two life stages[33,38,39,40] For this reason, the presence of an actively feeding larval stage has been hypothesised to be an ontogenetic constraint on the adult morphology, whereas the loss of an actively feeding larval stage has been suggested to promote morphological novelty[19,20,41,42] and drive increased rates of morphological evolution[11,21,22]. The anuran cranium comprises multiple osteological units with different functions, embryonic origins and types and timings of ossification[43,51,52,53]

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Conclusion