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The Evolution of Modularity in the Mammalian Skull I: Morphological Integration Patterns and Magnitudes

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Abstract

Morphological integration refers to the modular structuring of inter-trait relationships in an organism, which could bias the direction and rate of morphological change, either constraining or facilitating evolution along certain dimensions of the morphospace. Therefore, the description of patterns and magnitudes of morphological integration and the analysis of their evolutionary consequences are central to understand the evolution of complex traits. Here we analyze morphological integration in the skull of several mammalian orders, addressing the following questions: are there common patterns of inter-trait relationships? Are these patterns compatible with hypotheses based on shared development and function? Do morphological integration patterns and magnitudes vary in the same way across groups? We digitized more than 3,500 specimens spanning 15 mammalian orders, estimated the correspondent pooled within-group correlation and variance/covariance matrices for 35 skull traits and compared those matrices among the orders. We also compared observed patterns of integration to theoretical expectations based on common development and function. Our results point to a largely shared pattern of inter-trait correlations, implying that mammalian skull diversity has been produced upon a common covariance structure that remained similar for at least 65 million years. Comparisons with a rodent genetic variance/covariance matrix suggest that this broad similarity extends also to the genetic factors underlying phenotypic variation. In contrast to the relative constancy of inter-trait correlation/covariance patterns, magnitudes varied markedly across groups. Several morphological modules hypothesized from shared development and function were detected in the mammalian taxa studied. Our data provide evidence that mammalian skull evolution can be viewed as a history of inter-module parcellation, with the modules themselves being more clearly marked in those lineages with lower overall magnitude of integration. The implication of these findings is that the main evolutionary trend in the mammalian skull was one of decreasing the constraints to evolution by promoting a more modular architecture.

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Acknowledgements

We thank Campbell Rolian and Katherine Willmore for the opportunity to present this data in the 2008 AAPA meeting. Benedikt Hallgrímsson and 2 anonymous referees made constructive comments on an earlier version of this paper. We are also grateful to the people and institutions that provided generous help and access to mammal collections: E. Westwig, N. Simmons, R. Voss and R. MacPhee (AMNH); L. Tomsett, P. Jenkins and D. Hills (BMNH); B. Paterson, W. Stanley, and L. Heaney (FMNH); J. Chupasko and M. Omura (MCZ); M. Godinot, F. Renoult, C. Lefrève and J. Cuisin (MNHN); L. Salles, J. Oliveira, F. Barbosa, and S. Franco (MNRJ); S. Costa and J. de Queiroz (MPEG); Staff at the Museo de la Universidad Nacional Mayor de San Marcos; M. de Vivo and J. Gualda (MZUSP); H. van Grouw and B. Bekkum-Ansari (Naturalis); R. Thorington, R. Chapman and L. Gordon (NMNH); M. Harman (Powell-Cotton Museum); Georges Lenglet (RBINS); E. Gilissen and W. Wendelen (RMCA); R. Asher, I. Thomas and D. Willborn (ZMB); F. Smith and S. Tardif (University of Tennessee, and the Oak Ridge Associated Universities Marmoset Research Center); C. Zollikofer, M. Ponce de Léon and T. Jashashvili (Zürich Universität); R. Smith (Museu de Anatomia da UNIFESP); E. Liberti (Museu de Anatomia “Professor Alfonso Bovero”). This research was supported by grants and fellowships from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES), Conselho Nacional de Pesquisas (CNPq), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Fundação José Bonifácio (FUJB), Projeto de Conservação e Utilização Sustentável da Diversidade Biológica (PROBIO), and an American Museum of Natural History Collections Study Grant.

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  1. Laboratório de Evolução de Mamíferos, Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, CP 11.461, CEP 05508-090, Sao Paulo, SP, Brasil

    Arthur Porto, Felipe B. de Oliveira, Leila T. Shirai, Valderes De Conto & Gabriel Marroig

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  1. Arthur Porto
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  2. Felipe B. de Oliveira
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Correspondence to Gabriel Marroig.

Appendix

Appendix

Landmark abbreviations and definitions

Landmarks

Abbreviations

Landmarks

Position

IS

lntradentale superior

Midline

PM

Premaxillary-maxillary suture at the alveolus

Both sides

NSL

Nasale

Midline

NA

Nasion

Midline

BR

Bregma

Both sides

PT

Pterion

Both sides

ZS

Zygomaxillare superior

Both sides

ZI

Zygomaxillare inferior

Both sides

MT

Maxillary tuberosity

Both sides

PNS

Posterior nasal spine

Midline

APET

Anterior petrous temporal

Both sides

BA

Basion

Midline

OPI

Opisthion

Midline

EAM

Anterior external auditory meatus

Both sides

PEAM

Posterior external auditory meatus

Both sides

ZYGO

Inferior zygo-temporal suture

Both sides

TSP

Temporo-spheno-parietal junction

Both sides

TS

Temporo-sphenoidal junction at petrous

Both sides

JP

Jugular process

Both sides

LD

Lambda

Midline

AS

Asterion

Both sides

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Porto, A., de Oliveira, F.B., Shirai, L.T. et al. The Evolution of Modularity in the Mammalian Skull I: Morphological Integration Patterns and Magnitudes. Evol Biol 36, 118–135 (2009). https://doi.org/10.1007/s11692-008-9038-3

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