Developmental origin underlies evolutionary rate variation across the placental skull

Author:

Goswami Anjali12ORCID,Noirault Eve1,Coombs Ellen J.123,Clavel Julien4,Fabre Anne-Claire156ORCID,Halliday Thomas J. D.17ORCID,Churchill Morgan8,Curtis Abigail9,Watanabe Akinobu11011ORCID,Simmons Nancy B.12,Beatty Brian L.1310ORCID,Geisler Jonathan H.1310ORCID,Fox David L.14,Felice Ryan N.1215

Affiliation:

1. Department of Life Sciences, Natural History Museum, London SW7 5BD, UK

2. Department of Genetics, Evolution, and Environment, University College London, London WC1E 6BT, UK

3. Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA

4. Université Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, 69622 Villeurbanne, France

5. Naturhistorisches Museum Bern, 3005 Bern, Switzerland

6. Institute of Ecology and Evolution, University of Bern, 3012 Bern, Switzerland

7. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham B15 2TT, UK

8. Department of Biology, University of Wisconsin Oshkosh, Oshkosh, WI 54901, USA

9. Department of Biology, University of Washington, Seattle, WA 98195, USA

10. Department of Anatomy, College of Osteopathic Medicine, New York Institute of Technology, Old Westbury, NY 11568, USA

11. Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA

12. Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024, USA

13. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA

14. Department of Earth and Environmental Sciences, University of Minnesota, Minneapolis, MN 55455, USA

15. Centre for Integrative Anatomy, Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK

Abstract

The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation.This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

Funder

Horizon 2020 Framework Programme

H2020 European Research Council

National Science Foundation

Natural Environment Research Council

Gertner Scholar

Labex

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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