Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals

Abstract

The evolution of semi-independent modules is hypothesized to underlie the functional diversification of serially repeating (metameric) structures. The mammal vertebral column is a classic example of a metameric structure that is both modular, with well-defined morphological regions, and functionally differentiated. How the evolution of regions is related to their functional differentiation in the forerunners of mammals remains unclear. Here we gathered morphometric and biomechanical data on the presacral vertebrae of two extant species that bracket the synapsid–mammal transition and use the relationship between form and function to predict functional differentiation in extinct non-mammalian synapsids. The origin of vertebral functional diversity does not correlate with the evolution of new regions but appears late in synapsid evolution. This decoupling of regions from functional diversity implies that an adaptive trigger is needed to exploit existing modularity. We propose that the release of axial respiratory constraints, combined with selection for novel mammalian behaviours in Late Triassic cynodonts, drove the functional divergence of pre-existing morphological regions.

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Fig. 1: Comparison of morphological and functional variation.
Fig. 2: Relationship between regionalization of morphology and function.
Fig. 3: Morphological heterogeneity versus functional heterogeneity.
Fig. 4: Estimated intervertebral joint functional diversity.

Data availability

Raw data are available through Harvard Dataverse: https://doi.org/10.7910/DVN/YMUHLU.

Code availability

Code required for calculating functional distributions is provided in the supplementary materials.

Change history

  • 20 February 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

We thank E. Hanslowe, J. Josimovich, B. Falk and R. Reed at the United States Geological Survey Daniel Beard Center, Invasive Species Science Branch, for providing the tegu cadavers used in this study. The cat cadavers were purchased directly from Carolina Biological. For advice on the functional distribution method we thank D. Polly and for general research support we thank all members of the Pierce Lab, particularly P. Lai. This research was supported by an American Association of Anatomists Fellowship (K.E.J.), the Harvard College Research Program and Museum of Comparative Zoology Grants-In-Aid of Undergraduate Research (S.G.), Harvard University (S.E.P), NSF EAR-1524938 (K.D.A.) and NSF EAR-1524523 (S.E.P.).

Author information

S.E.P. and K.E.J. conceived and designed the study. S.G. conducted the ex vivo bending experiments in consultation with K.E.J. and S.E.P. and in partial fulfilment of an undergraduate senior thesis. K.E.J. analysed the morphological and functional data, interpreted the data, made the figures and drafted the manuscript. S.E.P. interpreted the data and drafted the manuscript. All authors edited the manuscript and gave final approval for publication.

Correspondence to Katrina E. Jones or Stephanie E. Pierce.

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Jones, K.E., Gonzalez, S., Angielczyk, K.D. et al. Regionalization of the axial skeleton predates functional adaptation in the forerunners of mammals. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-1094-9

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