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.

Biting disrupts integration to spur skull evolution in eels

“…Within both suction feeders and biters, we compared the overall magnitude of evolutionary integration between mechanical units to the level of evolutionary integration within them. We evaluated integration between mechanical units as the mean of the absolute values of their three evolutionary correlations, following Young and Hallgrimsson 11 . Integration within a mechanical unit was determined as the mean magnitude of evolutionary correlation between morphological traits within that unit, where the pairwise evolutionary correlations between traits were estimated using a modelfitting and model-averaging approach similar to the method described above.…”

“…Overlap among structures in function creates dependence, known as functional integration, which can shape the potential for morphological differences to evolve 6,7 . Shared genes and developmental pathways can bias the kinds of new phenotypic variants that arise by mutation [8][9][10][11][12] , but the resulting combinations of structures must be able to execute their shared function [1][2][3][4]6,7 (for example, a change in the shape of the hyoid must allow for proper orientation with the jaws and operculum to maintain effective oral expansion). Therefore, functional integration imposes internal selection on morphological variety, culling forms that impair function 7,8,13 and leading to selective covariance among traits 14 .…”

“…The origin of one of these integrationdisrupting innovations may therefore act as a catalyst of morphological diversification, allowing structures to evolve independently of one another, to accumulate differences among species at a faster rate and to reach more extreme forms 1,3,4,15,17 . Few empirical studies, however, have connected such innovations-and their associated changes in the strength of functional integration-with shifts in evolutionary integration (that is, correlations between evolutionary change in structures or suites of structures 9,11 ), rates of evolution and morphospace occupation (but see related studies by Monteiro et al 22 and Claverie and Patek 23 ).…”

The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

“…Foreand hindlimbs show strong integration within each limb, but weak or no integration across the limbs (24,26,38). Different again are the placental mammals, which show strong within-limb and between-limb integration, reflecting both functional associations and serial homology (28). These differences in integration as measured from adult morphology correspond with heterochronic shifts in ossification (25) and in gene-expression patterns (39).…”

“…Much recent work has focused on characterizing large-scale patterns of trait relationships through comparative studies of extant and fossil taxa (11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23), in some cases demonstrating shifts in phenotypic integration related to changes in development (24)(25)(26), function (27)(28)(29), and environment (30)(31)(32)(33). Although focused overwhelmingly on model organisms, these studies provide a foundation for understanding how phenotypic integration changes through ontogenetic and evolutionary time and how it relates to myriad factors shaping morphological evolution.…”