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Initial radiation of jaws demonstrated stability despite faunal and environmental change

Abstract

More than 99 per cent of the roughly 58,000 living vertebrate species have jaws1. This major clade, whose members are collectively known as gnathostomes (‘jawed mouths’), made its earliest definitive appearance in the Silurian period, 444–416 million years (Myr) ago, with both the origin of the modern (crown-group) radiation and the presumptive invasion of land occurring by the end of the Devonian period2 (359 Myr ago). These events coincided with a major faunal shift that remains apparent today: the transition from Silurian ecosystems dominated by jawless fishes (agnathans) to younger assemblages composed almost exclusively of gnathostomes2,3. This pattern has inspired several qualitative descriptions of the trophic radiation and ecological ascendance of the earliest jawed vertebrates3,4,5,6,7. Here we present a quantitative analysis of functional variation in early gnathostome mandibular elements, placing constraints on our understanding of evolutionary patterns during this critical interval. We document an initial increase in functional disparity in the Silurian that stabilized by the first stage of the Devonian, before the occurrence of an Emsian (400 Myr ago) oxygenation event implicated in the trophic radiation of vertebrates8. Subsequent taxonomic diversification during the Devonian did not result in increased functional variation; instead, new taxa revisited and elaborated on established mandibular designs. Devonian functional space is dominated by lobe-finned fishes and ‘placoderms’; high disparity within the latter implies considerable trophic innovation among jaw-bearing stem gnathostomes. By contrast, the major groups of living vertebrates—ray-finned fishes and tetrapods—show surprisingly conservative mandibular morphologies with little indication of functional diversification or innovation. Devonian gnathostomes reached a point where they ceased to accrue further mandibular functional disparity before becoming taxonomic dominants relative to ‘ostracoderm’-grade jawless fishes, providing a new perspective on classic adaptive hypotheses concerning this fundamental shift in vertebrate biodiversity.

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Figure 1: Functional mandibular disparity among Silurian/Devonian gnathostomes.
Figure 2: Patterns of functional morphospace occupation for jawed vertebrates during the late Silurian and Devonian.

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Acknowledgements

We thank P. Donoghue, M. Rücklin and M. Ruta for discussions. This work was supported by Royal Society and Marie-Curie Actions fellowships, awarded to P.S.L.A.; a Fell Fund award to M.F.; NERC grant NE/G016623/1, awarded in part to E.J.R.; and a FQRNT postdoctoral fellowship, to M.D.B.

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Authors and Affiliations

Authors

Contributions

P.S.L.A. designed and led the study, developed the biomechanical traits, collected data, performed the disparity and multivariate analyses, and wrote the paper. M.F. gathered data, wrote analytical code, performed the faunal analyses, drafted figures and wrote the paper. M.D.B. gathered data and produced illustrations. E.J.R. gave advice on biomechanical theory. All authors contributed to interpretation of the results and edited the paper.

Corresponding author

Correspondence to Philip S. L. Anderson.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Text, Supplementary Figures 1-13 with legends, Supplementary Tables 1-12 and additional references. (PDF 1889 kb)

Supplementary Data

This file contains raw data analyzed in this study. These include: averaged biomechanical metrics for each genus, multivariate coordinate scores for each genus taken from the NMDS, faunal composition data used for the intrafaunal comparisons. (XLS 212 kb)

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Anderson, P., Friedman, M., Brazeau, M. et al. Initial radiation of jaws demonstrated stability despite faunal and environmental change. Nature 476, 206–209 (2011). https://doi.org/10.1038/nature10207

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