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Multiple paths to morphological diversification during the origin of amniotes

Abstract

Early terrestrial vertebrates (amniotes) provide a classic example of diversification following adaptive zone invasion. The initial terrestrialization of vertebrates was closely followed by dietary diversification, as evidenced by a proliferation of craniomandibular and dental adaptations. However, morphological evolution of early amniotes has received limited study, in analyses with restricted taxonomic scope, leaving substantial questions about the dynamics of this important terrestrial radiation. We use novel analyses of discrete characters to quantify variation in evolutionary rates and constraints during diversification of the amniote feeding apparatus. We find evidence for an early burst, comprising high rates of anatomical change that decelerated through time, giving way to a background of saturated morphological evolution. Subsequent expansions of phenotypic diversity were not associated with increased evolutionary rates. Instead, variation in the mode of evolution became important, with groups representing independent origins of herbivory evolving distinctive, group-specific morphologies and thereby exploring novel character-state spaces. Our findings indicate the importance of plant–animal interactions in structuring the earliest radiation of amniotes and demonstrate the importance of variation in modes of phenotypic divergence during a major evolutionary radiation.

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Fig. 1: Summary of the supertree used in the study.
Fig. 2: Rates of dental evolution and disparity during the origin of amniotes.
Fig. 3: Comparisons of patristic morphological distances to pairwise morphological dissimilarity for faunivorous and herbivorous amniotes.

Data availability

All data analysed in this study are available in Supplementary Data 16.

Code availability

The analysis code is available in Supplementary Data 7.

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Acknowledgements

N.B. thanks D. Button, M. Ezcurra, D. Ford, C. Kammerer, J. Ponstein and X.-C. Wu for helpful discussions and assistance with character scores; A. S. Murray and M. Day (Natural History Museum London), D. Schwarz (Museum für Naturkunde, Berlin), N.-E. Jalil (Muséum National d’Histoire Naturelle, Paris), S. Jirah and B. Zipfel (Evolutionary Studies Institute, Johannesburg), C. Mehling and M. Norrell (American Museum of Natural History, New York), J. Cundiff (Museum of Comparative Zoology, Harvard) and W. Simpson (Field Museum of Natural History, Chicago) for access to specimens and assistance during visits to collections. N.B.’s research was funded by Deutsche Forschungsgemeinschaft grant number BR 5724/1-1, Palaeontological Association Research grant number PA-RG201901 and a Collections Study Grant from the American Museum of Natural History. Parts of this work were funded by the European Union’s Horizon 2020 research and innovation program 2014–2018 under grant agreement 677774 (European Research Council (ERC) Starting Grant: TEMPO) to R.J.B.

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N.B. conceptualized the project, and collected and analysed the data. N.B. and R.J.B. developed the methodology and wrote the manuscript.

Corresponding author

Correspondence to Neil Brocklehurst.

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The authors declare no competing interests.

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Peer review information Nature Ecology & Evolution thanks Peter Wagner and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Supplementary information

Supplementary Information

Supplementary Datasets 1 and 2, Figs. 1 and 2, Table 1, and Data 1–7.

Reporting Summary

Peer Review Information

Supplementary Table 1

By-interval t tests, comparing the disparity values obtained at each time slice to those of the preceding slice, and identifying intervals where significant shifts occurred. Intervals with significant shifts (P < 0.05) are highlighted in yellow.

Supplementary Data 1

Character taxon matrix and MrBayes commands for time calibration of the tree, constraining the topology to that of the main text supertree.

Supplementary Data 2

Character taxon matrix and MrBayes commands for time calibration of the tree, constraining the topology to that of Ford and Benson51.

Supplementary Data 3

Maximum clade credibility time-calibrated tree of the main text supertree.

Supplementary Data 4

Maximum clade credibility time-calibrated tree of the supertree constrained to the Ford and Benson topology.

Supplementary Data 5

Maximum clade credibility tree of the main text supertree, with branch lengths representing morphological change instead of time.

Supplementary Data 6

First and last appearances and diet of taxa.

Supplementary Data 7

Analysis script.

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Brocklehurst, N., Benson, R.J. Multiple paths to morphological diversification during the origin of amniotes. Nat Ecol Evol 5, 1243–1249 (2021). https://doi.org/10.1038/s41559-021-01516-x

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