Chapter 12. Evolution of Covariance in the Mammalian Skull

  1. Gregory Bock Organizer and
  2. Jamie Goode
  1. Benedikt Hallgrimsson1,
  2. Daniel E. Lieberman Chair1,2,
  3. Nathan M. Young1,3,
  4. Trish Parsons1 and
  5. Steven Wat1

Published Online: 11 JUN 2007

DOI: 10.1002/9780470319390.ch12

Tinkering: The Microevolution of Development: Novartis Foundation Symposium 284

Tinkering: The Microevolution of Development: Novartis Foundation Symposium 284

How to Cite

Hallgrimsson, B., Lieberman, D. E., Young, N. M., Parsons, T. and Wat, S. (2006) Evolution of Covariance in the Mammalian Skull, in Tinkering: The Microevolution of Development: Novartis Foundation Symposium 284 (eds G. Bock and J. Goode), John Wiley & Sons, Ltd, Chichester, UK. doi: 10.1002/9780470319390.ch12

Author Information

  1. 1

    Department of Cell Biology, and Bone and Joint Institute, University of Calgary, 3330 Hospital Drive NW, Calgary, Alverta T2N 4N1, Canada

  2. 2

    Departments of Anthropology and Organismic and Evolutionary Biology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA

  3. 3

    Department of Surgery, Stanford University, Stanford, CA 94305–5148, USA

Publication History

  1. Published Online: 11 JUN 2007
  2. Published Print: 8 JUN 2006

Book Series:

  1. Novartis Foundation Symposia

Book Series Editors:

  1. Novartis Foundation

ISBN Information

Print ISBN: 9780470034293

Online ISBN: 9780470319390



  • morphological integration;
  • covariance structure;
  • mouse models;
  • skull;
  • A/WySn;
  • brachymorph;
  • mceph


The skull is a developmentally complex and highly integrated structure. Integration, which is manifested as covariance among structures, enables the skull and associated soft tissues to maintain function both across ontogeny within individuals and across the ranges of size and shape variation among individuals. Integration also contributes to evolvability by structuring the phenotypic expression of genetic variation. We argue that the pattern of covariation seen in complex phenotypes such as the skull results from the overlaying of variation introduced by developmental and environmental factors at different stages of development. Much like a palimpsest, the covariation structure of an adult skull represents the summed imprint of a succession of effects, each of which leaves a distinctive covariation signal determined by the specific set of developmental interactions involved. Covariance evolves either by altering the variance of one of these sequential effects or through the introduction of a novel covariance producing effect. Either way is consistent with the notion that evolutionary change occurs through tinkering. We illustrate these principles through analyses of how genetic perturbations acting at different developmental stages (embryonic, fetal, and postnatal) influence the covariance structure of adult mouse skulls. As predicted by the model, the results illustrate the intimate relationship between the modulation of variance and the expression of covariance. The results also demonstrate that covariance patterns have a complex relationship to the underlying developmental architecture, thus highlighting problems with making inferences about developmental relationships (e.g. modularity) based on covariation.