Evolutionary Biology

, Volume 36, Issue 1, pp 136–148 | Cite as

The Evolution of Modularity in the Mammalian Skull II: Evolutionary Consequences

  • Gabriel MarroigEmail author
  • Leila T. Shirai
  • Arthur Porto
  • Felipe B. de Oliveira
  • Valderes De Conto
Research Article


Changes in patterns and magnitudes of integration may influence the ability of a species to respond to selection. Consequently, modularity has often been linked to the concept of evolvability, but their relationship has rarely been tested empirically. One possible explanation is the lack of analytical tools to compare patterns and magnitudes of integration among diverse groups that explicitly relate these aspects to the quantitative genetics framework. We apply such framework here using the multivariate response to selection equation to simulate the evolutionary behavior of several mammalian orders in terms of their flexibility, evolvability and constraints in the skull. We interpreted these simulation results in light of the integration patterns and magnitudes of the same mammalian groups, described in a companion paper. We found that larger magnitudes of integration were associated with a blur of the modules in the skull and to larger portions of the total variation explained by size variation, which in turn can exert a strong evolutionary constraint, thus decreasing the evolutionary flexibility. Conversely, lower overall magnitudes of integration were associated with distinct modules in the skull, to smaller fraction of the total variation associated with size and, consequently, to weaker constraints and more evolutionary flexibility. Flexibility and constraints are, therefore, two sides of the same coin and we found them to be quite variable among mammals. Neither the overall magnitude of morphological integration, the modularity itself, nor its consequences in terms of constraints and flexibility, were associated with absolute size of the organisms, but were strongly associated with the proportion of the total variation in skull morphology captured by size. Therefore, the history of the mammalian skull is marked by a trade-off between modularity and evolvability. Our data provide evidence that, despite the stasis in integration patterns, the plasticity in the magnitude of integration in the skull had important consequences in terms of evolutionary flexibility of the mammalian lineages.


Morphological integration Constraints Evolvability Selection Evolutionary flexibility 



We thank Campbell Rolian and Katherine Willmore for the opportunity to present this data in the 2008 AAPA meeting. Many thanks also to an anonymous reviewer for comments that helped us to improve an earlier version of the text, and to Thomas Hansen, for his suggestion of the term flexibility for the correlation between selection vector and the evolutionary responses. We are also grateful to those people and institutions that provided generous help and access to mammal collections: E. Westwig, 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. Gualba (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), and an American Museum of Natural History Collections Study Grant.


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Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Gabriel Marroig
    • 1
    Email author
  • Leila T. Shirai
    • 1
  • Arthur Porto
    • 1
  • Felipe B. de Oliveira
    • 1
  • Valderes De Conto
    • 1
  1. 1.Laboratório de Evolução de Mamíferos, Departamento de BiologiaInstituto de Biociências, Universidade de São PauloSão PauloBrazil

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