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.
This study measures the correlation between within- and among-individual variance to gain a greater understanding of the relationship of the underlying mechanisms governing developmental stability and canalization. Twenty-six landmarks were digitized in three dimensions from the crania of 228 adult macaques from Cayo Santiago. The phenotypic variance between individuals was measured and divided into its genetic and environmental components using matriline information. Within-individual variance was measured as the fluctuating asymmetry between bilateral landmarks. We found positive and significant correlations between the phenotypic, environmental, and fluctuating asymmetry variances for interlandmark distances. We also found low but significant correspondences between the covariation structures of the three variability components using both Procrustes and interlandmark distance data. Therefore, we find that in macaque skulls traits that exhibit greater levels of asymmetry deviations also exhibit greater levels of environmental variance, and that the covariances of absolute symmetry deviations partly correspond to covariances of mean deviations at the individual level. These results suggest that the underlying processes that determine canalization and developmental stability are at least partly overlapping. However, the low correlations reported here are also evidence for a degree of independence between these variability components.
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