Serial Homology and the Evolution of Mammalian Limb Covariation Structure

Abstract

The tetrapod forelimb and hindlimb are serially homologous structures that share a broad range of developmental pathways responsible for their patterning and outgrowth. Covariation between limbs, which can introduce constraints on the production of variation, is related to the duplication of these developmental factors. Despite this constraint, there is remarkable diversity in limb morphology, with a variety of functional relationships between and within forelimb and hindlimb elements. Here we assess a hierarchical model of limb covariation structure based on shared developmental factors. We also test whether selection for morphologically divergent forelimbs or hindlimbs is associated with reduced covariation between limbs. Our sample includes primates, murines, a carnivoran, and a chiropteran that exhibit varying degrees of forelimb and hindlimb specialization, limb size divergence, and/or phylogenetic relatedness. We analyze the pattern and significance of between-limb morphological covariation with linear distance data collected using standard morphometric techniques and analyzed by matrix correlations, eigenanalysis, and partial correlations. Results support a common limb covariation structure across these taxa and reduced covariation between limbs in nonquadruped species. This result indicates that diversity in limb morphology has evolved without signficant modifications to a common covariation structure but that the higher degree of functional limb divergence in bats and, to some extent, gibbons is associated with weaker integration between limbs. This result supports the hypothesis that limb divergence, particularly selection for increased functional specialization, involves the reduction of developmental factors common to both limbs, thereby reducing covariation.

Measuring Morphological Integration Using Eigenvalue Variance

“…Eigenvalue variance is frequently applied to measure phenotypic integration in wide range of fields (e.g., Herrera et al 2002;Peres-Neto and Magnan 2004;Hallgrimsson et al 2004;Young and Hallgrimsson 2005;Hallgrimsson et al 2006;Parsons and Robinson 2006;Young 2006), and also indirectly to assess the effective number of independent variables in a correlation matrix on a continuous scale (Wagner et al 2008). The latter purpose was originally developed to determine the number of independent tests to calculate the significance threshold in QTL mapping based on the Bonferroni adjustment (Cheverud 2001;Nyholt 2004).…”

Building Developmental Integration into Functional Systems: Function-Induced Integration of Mandibular Shape

“…This matrix can be obtained by inverting the observed correlation matrix and rescaling the values so that elements along the diagonal are all 1.0. Magwene (2001) showed that graphical modeling can be useful for studying morphological integration, clarifying both concepts of modularity and revealing the structure of integration, and several recent empirical studies have used this method to test theories of integration/modularity (e.g., Young 2004;Young and Hallgrímsson 2005;Polanski and Franciscus 2006;Allen 2008;Lawler 2008).…”

Phenotypic Variability: Its Components, Measurement and Underlying Developmental Processes

“…The structures that comprise the cranium will show a higher degree of inter-relatedness with other structures of the head than they will with limb traits, and the reverse is true for the limbs. Cranial and limb modules may form due to the physical adjacency of the structures, shared developmental origins, or shared functional demands (Young and Hallgrímsson 2005).…”