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Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

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Abstract

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.

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Acknowledgments

We thank R. Abel and S. Walsh for providing training and support to E.S. on the Natural History Museum X-ray computed tomography scanner. We are grateful to P. Withers and C. Martin for access to resources in the Henry Mosley HRXCT Facility, Manchester, and to D. San Mauro, S. D. Biju and R. G. Kamei for important practical assistance. E.S. thanks L. Monteiro, T.J. Sanger, H. Maddin, B. Sidlauskas, T. Stayton and D.C. Adams for helpful discussion and critique of the study, as well as the reviewers for their helpful comments. We thank the many researchers, curators, institutions and authorities (too numerous to mention individually) who have facilitated the collection of or access to caecilian specimens without which this project would not have been possible. E.S. was funded by NERC CASE Studentship NE/F009011/1.

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  1. Emma Sherratt

    Present address: Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, 50011, USA

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  1. Department of Zoology (Currently the Department of Life Sciences), The Natural History Museum, London, SW7 5BD, UK

    Emma Sherratt, David J. Gower & Mark Wilkinson

  2. Faculty of Life Sciences, University of Manchester, Oxford Road, Manchester, M13 9PT, UK

    Emma Sherratt & Christian Peter Klingenberg

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Sherratt, E., Gower, D.J., Klingenberg, C.P. et al. Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona). Evol Biol 41, 528–545 (2014). https://doi.org/10.1007/s11692-014-9287-2

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