Abstract

Adaptation is the fundamental driver of functional and biomechanical evolution. Accordingly, the states of biomechanical traits (absolute or relative trait values) have long been used as proxies for adaptations in response to direct selection. However, ignoring evolutionary history, in particular ancestry, passage of time and the rate of evolution, can be misleading. Here, we apply a recently developed phylogenetic statistical approach using significant rate shifts to detect instances of exceptional rates of adaptive changes in bite force in a large group of terrestrial vertebrates, the amniotes. Our results show that bite force in amniotes evolved through multiple bursts of exceptional rates of adaptive changes, whereby whole groups-including Darwin's finches, maniraptoran dinosaurs (group of non-avian dinosaurs including birds), anthropoids and hominins (fossil and modern humans)-experienced significant rate increases compared to the background rate. However, in most parts of the amniote tree of life, we find no exceptional rate increases, indicating that coevolution with body size was primarily responsible for the patterns observed in bite force. Our approach represents a template for future studies in functional morphology and biomechanics, where exceptional rates of adaptive changes can be quantified and potentially linked to specific ecological factors underpinning major evolutionary radiations.

Highlights

  • Adaptation is the fundamental driver of functional and biomechanical evolution

  • We tested for instances of exceptional bursts of evolutionary change in bite force based on rate shifts along branches on the phylogeny [9], based on the premise that phenotypic changes owing to adaptations would be proportional to r

  • Our results show that bite force evolved through multiple bursts of exceptional rates of adaptive changes, whereby whole groups experienced rate increases of bite force evolution compared to the background rate across the entire amniote tree

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Summary

Background

Adaptation is the fundamental driver of functional and biomechanical evolution. Measures of biomechanical performance—e.g. bite force—characterize and quantify specific functional performances to fulfil ecological demand— e.g. diet [1,2]. We test the hypothesis that instances of exceptional rates of adaptive changes have shaped the observed diversity in biomechanical traits focusing on bite force evolution. Bite force relates to species’ niche and feeding ecology, is correlated with several ecological and behavioural traits [28,29,30,31] and is widely available from the literature across several fields of study (e.g. biomechanics, ecology, palaeobiology) for a broad sample of the tree of life, making it an ideal biomechanical trait to test our hypothesis using a phylogenetic framework To this end, we assembled, to the best of our knowledge, the largest dataset of bite forces collected to date for amniotes, both extinct (including non-avian dinosaurs, sabre-toothed cats and fossil hominins) and extant. We tested for instances of exceptional bursts of evolutionary change in bite force based on rate shifts along branches on the phylogeny [9], based on the premise that phenotypic changes owing to adaptations ( potentially as a response to strong selective pressure) would be proportional to r.

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14. Walker J et al 2007 A general model of functional
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