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Interrelationships Between Bones, Muscles, and Performance: Biting in the Lizard Tupinambis merianae

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Abstract

The origins of and potential constraints on the evolution of phenotypic diversity remain one of the central questions in evolutionary biology. The vertebrate skeleton is governed by historical, developmental, architectural, and functional constraints that all play a role in establishing its final form. Whereas the factors underlying shape variation in single bones are fairly well understood, this is less so the case for complex assemblages of bones as observed in the cranium or mandible. It is often suggested that the final phenotype must reflect the mechanical constraints imposed by the loading of the skeleton as bones remodel to withstand loading. Yet, in the cranium, in contrast to the mandible, the final phenotype is likely constrained by demands other than loading including the protection of sensory systems and the brain. Architectural design constraints may further limit the final form of complex units like the vertebrate cranium. Here we use geometric morphometric approaches to quantify the shape of the cranium and mandible in a lizard and test whether the observed shape co-varies with both the muscles attaching to these structures as well as functional traits such as bite force. Our results show that co-variation between the cranium and mandible is significant and likely driven by the muscles that link the two systems. Moreover, our results show that the patterns of co-variation are stronger between the mandible and ventral side of the cranium. Muscular cross sectional areas, bite force, and the ventral side of the cranium, also co-vary more than the dorsal side of the cranium does with muscle properties and function. Finally, our results show sex-specific patterns of co-variation with males showing a stronger degree of integration between the cranium, mandible, muscles and bite force suggesting that constraints on bite force drive the evolution of cranial shape to a greater extent in males compared to females.

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Acknowledgments

The authors would like to thank two anonymous reviewers for constructive comments on a previous version of the manuscript; we thank Jose Eduardo de Carvalho, Ananda Brito and Carlos Carlos Navas for help in collecting the data. D.V.A. was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), and Fundação para o Desenvolvimento da Universidade Estudial Paulista (FUNDUNESP); K.H. is a postdoctoral fellow of the fund for scientific research, Flanders, Belgium (FWO-Vl); A-C. F is supported by the Fondation Fyssen.

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Authors and Affiliations

  1. Evolutionary Anthropology, Duke University, Durham, NC, 27708-0383, USA

    Anne-Claire Fabre

  2. Departamento de Zoologia, Universidade Estadual Paulista, c. p. 199, Rio Claro, São Paulo, 13506-900, Brazil

    Denis V. Andrade

  3. Department of Biology, University of Antwerp, Universiteitsplein 1, 2610, Antwerpen, Belgium

    Katleen Huyghe

  4. Origine, Structure et Evolution de la Biodiversité, UMR 7205, CNRS/MNHN, 45 rue Buffon, 75005, Paris, France

    Raphael Cornette

  5. UMR CNRS/MNHN 7179, “Mécanismes adaptatifs: des organismes aux communautés”, 55 Rue Buffon, 75005, Paris, France

    Anthony Herrel

  6. Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, 9000, Ghent, Belgium

    Anthony Herrel

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  1. Anne-Claire Fabre
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  2. Denis V. Andrade
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Correspondence to Anthony Herrel.

Electronic supplementary material

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11692_2014_9286_MOESM1_ESM.tif

Figure S1: Results of a two-block partial least squares analysis performed on data for males only. A) partial least squares analysis for the mandible and the shape of the in dorsal view; B) partial least squares analysis for the mandible and the shape of the in ventral view. Illustrated are the landmarks taken on the cranium and mandible as well as the shapes representing the extremes along the first PLS axis (red = positive; blue = negative). (TIFF 5343 kb)

11692_2014_9286_MOESM2_ESM.tif

Figure S2: Results of a two-block partial least squares analysis performed on data for females only. A) partial least squares analysis for the mandible and the shape of the in dorsal view; B) partial least squares analysis for the mandible and the shape of the in ventral view. Illustrated are the landmarks taken on the cranium and mandible as well as the shapes representing the extremes along the first PLS axis (red = positive; blue = negative). (TIFF 5340 kb)

11692_2014_9286_MOESM3_ESM.tif

Figure S3: Results of a two-block partial least squares analysis performed on data for males only. A) covariation between the dorsal side of the skull and the muscle cross sectional areas; B) covariation between the ventral side of the skull and the muscle cross sectional areas; C) covariation between the mandible and the muscle cross sectional areas. Illustrated are the landmarks taken on the cranium and mandible as well as the shapes representing the extremes along the first PLS axis (red = positive; blue = negative). Closed symbols represent males, open symbols females. (TIFF 4817 kb)

11692_2014_9286_MOESM4_ESM.tif

Figure S4: Results of a two-block partial least squares analysis performed on data for females only. A) covariation between the dorsal side of the skull and the muscle cross sectional areas; B) covariation between the ventral side of the skull and the muscle cross sectional areas; C) covariation between the mandible and the muscle cross sectional areas. Illustrated are the landmarks taken on the cranium and mandible as well as the shapes representing the extremes along the first PLS axis (red = positive; blue = negative). Closed symbols represent males, open symbols females. (TIFF 4871 kb)

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Fabre, AC., Andrade, D.V., Huyghe, K. et al. Interrelationships Between Bones, Muscles, and Performance: Biting in the Lizard Tupinambis merianae . Evol Biol 41, 518–527 (2014). https://doi.org/10.1007/s11692-014-9286-3

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