First evidence of convergent lifestyle signal in reptile skull roof microanatomy

Abstract Background The study of convergently acquired adaptations allows fundamental insight into life’s evolutionary history. Within lepidosaur reptiles—i.e. lizards, tuatara, and snakes—a fully fossorial (‘burrowing’) lifestyle has independently evolved in most major clades. However, despite thei...

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Main Authors: Roy Ebel, Johannes Müller, Till Ramm, Christy Hipsley, Eli Amson
Format: Article
Language:English
Published: BMC 2020-11-01
Series:BMC Biology
Subjects:
Online Access:https://doi.org/10.1186/s12915-020-00908-y
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author Roy Ebel
Johannes Müller
Till Ramm
Christy Hipsley
Eli Amson
author_facet Roy Ebel
Johannes Müller
Till Ramm
Christy Hipsley
Eli Amson
author_sort Roy Ebel
collection DOAJ
description Abstract Background The study of convergently acquired adaptations allows fundamental insight into life’s evolutionary history. Within lepidosaur reptiles—i.e. lizards, tuatara, and snakes—a fully fossorial (‘burrowing’) lifestyle has independently evolved in most major clades. However, despite their consistent use of the skull as a digging tool, cranial modifications common to all these lineages are yet to be found. In particular, bone microanatomy, although highly diagnostic for lifestyle, remains unexplored in the lepidosaur cranium. This constitutes a key gap in our understanding of their complexly interwoven ecology, morphology, and evolution. In order to bridge this gap, we reconstructed the acquisition of a fossorial lifestyle in 2813 lepidosaurs and assessed the skull roof compactness from microCT cross-sections in a representative subset (n = 99). We tested this and five macroscopic morphological traits for their convergent evolution. Results We found that fossoriality evolved independently in 54 lepidosaur lineages. Furthermore, a highly compact skull roof, small skull diameter, elongate cranium, and low length ratio of frontal and parietal were repeatedly acquired in concert with a fossorial lifestyle. Conclusions We report a novel case of convergence that concerns lepidosaur diversity as a whole. Our findings further indicate an early evolution of fossorial modifications in the amphisbaenian ‘worm-lizards’ and support a fossorial origin for snakes. Nonetheless, our results suggest distinct evolutionary pathways between fossorial lizards and snakes through different contingencies. We thus provide novel insights into the evolutionary mechanisms and constraints underlying amniote diversity and a powerful tool for the reconstruction of extinct reptile ecology.
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spelling doaj.art-b67245dcc3c44e7e8a59413142d6e5e42022-12-21T22:55:00ZengBMCBMC Biology1741-70072020-11-0118111810.1186/s12915-020-00908-yFirst evidence of convergent lifestyle signal in reptile skull roof microanatomyRoy Ebel0Johannes Müller1Till Ramm2Christy Hipsley3Eli Amson4Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceSchool of BioSciences, The University of MelbourneMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity ScienceAbstract Background The study of convergently acquired adaptations allows fundamental insight into life’s evolutionary history. Within lepidosaur reptiles—i.e. lizards, tuatara, and snakes—a fully fossorial (‘burrowing’) lifestyle has independently evolved in most major clades. However, despite their consistent use of the skull as a digging tool, cranial modifications common to all these lineages are yet to be found. In particular, bone microanatomy, although highly diagnostic for lifestyle, remains unexplored in the lepidosaur cranium. This constitutes a key gap in our understanding of their complexly interwoven ecology, morphology, and evolution. In order to bridge this gap, we reconstructed the acquisition of a fossorial lifestyle in 2813 lepidosaurs and assessed the skull roof compactness from microCT cross-sections in a representative subset (n = 99). We tested this and five macroscopic morphological traits for their convergent evolution. Results We found that fossoriality evolved independently in 54 lepidosaur lineages. Furthermore, a highly compact skull roof, small skull diameter, elongate cranium, and low length ratio of frontal and parietal were repeatedly acquired in concert with a fossorial lifestyle. Conclusions We report a novel case of convergence that concerns lepidosaur diversity as a whole. Our findings further indicate an early evolution of fossorial modifications in the amphisbaenian ‘worm-lizards’ and support a fossorial origin for snakes. Nonetheless, our results suggest distinct evolutionary pathways between fossorial lizards and snakes through different contingencies. We thus provide novel insights into the evolutionary mechanisms and constraints underlying amniote diversity and a powerful tool for the reconstruction of extinct reptile ecology.https://doi.org/10.1186/s12915-020-00908-yConvergent evolutionBoneMicroanatomySkull roofFossorialLepidosaur
spellingShingle Roy Ebel
Johannes Müller
Till Ramm
Christy Hipsley
Eli Amson
First evidence of convergent lifestyle signal in reptile skull roof microanatomy
BMC Biology
Convergent evolution
Bone
Microanatomy
Skull roof
Fossorial
Lepidosaur
title First evidence of convergent lifestyle signal in reptile skull roof microanatomy
title_full First evidence of convergent lifestyle signal in reptile skull roof microanatomy
title_fullStr First evidence of convergent lifestyle signal in reptile skull roof microanatomy
title_full_unstemmed First evidence of convergent lifestyle signal in reptile skull roof microanatomy
title_short First evidence of convergent lifestyle signal in reptile skull roof microanatomy
title_sort first evidence of convergent lifestyle signal in reptile skull roof microanatomy
topic Convergent evolution
Bone
Microanatomy
Skull roof
Fossorial
Lepidosaur
url https://doi.org/10.1186/s12915-020-00908-y
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