Developmental origin underlies evolutionary rate variation across the placental skull

Anjali Goswami, Eve Noirault, Ellen J. Coombs, Julien Clavel, Anne Claire Fabre, Thomas J.D. Halliday, Morgan Churchill, Abigail Curtis, Akinobu Watanabe, Nancy B. Simmons, Brian L. Beatty, Jonathan H. Geisler, David L. Fox, Ryan N. Felice

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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'.

Original languageEnglish (US)
Article number20220083
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume378
Issue number1880
DOIs
StatePublished - Jul 3 2023

Bibliographical note

Funding Information:
This work was supported by funding from European Research Council grant STG-2014-637171 (to A.G.), National Science Foundation SF-EAR grant 1349607 (J.G., B.B., A.G., M.C.), Gerstner Scholar Postdoctoral Research Fellowship (A.C., N.S.), Natural Environment Research Council Doctoral Training Partnership training grant NE/L002485/1 (E.C.), National Science Foundation EAR 1338262 (D.L.F.), Horizon 2020 MCSA Fellowship IF 797373-EVOTOOLS (to J.C.) and Labex BCDiv 10-LABX-0003 (to A.C.F.). Acknowledgements

Publisher Copyright:
© 2023 The Author(s).

Keywords

  • cranial neural crest
  • development
  • ecology
  • morphometrics
  • skull evolution

PubMed: MeSH publication types

  • Journal Article
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, Non-U.S. Gov't

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