Serial homology and the evolution of mammalian limb covariation structure

Department of Cell Biology and Anatomy, University of Calgary, Health Sciences Centre, 3330 Hospital Drive NW, Calgary, Alberta T2N 4N1, Canada.
Evolution (Impact Factor: 4.66). 01/2006; 59(12):2691-704. DOI: 10.1554/05-233.1
Source: PubMed

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.

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Available from: Nathan M. Young, Jul 14, 2015
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    • "The dots represent landmarks points. The xy coordinates of these landmarks are the raw data in shape analyses (redrawn from Young and Hallgrímsson 2005) Evol Biol "
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    ABSTRACT: Correlation patterns have been widely used in evolutionary studies for exploring the role of development in channelling morphological evolution. The approach was firstly introduced by Olson and Miller in the 1950s, but it did not gain prominence until the 1980s, due to some extent to Gould and Lewontin’s (Proc R Soc Lond B 205:581–598, 1979) assertion of the importance of considering organisms as integrated entities, where the internal organization of a structure, and not only the selective regime acting upon it, would play a fundamental role in its evolution. Here we show that this approach, mainly focused on the study of small, quantitative shape changes of existing structures, does not deal with a fundamental aspect of developmental systems, that is, their intrinsic capacity of originating morphological novelties. We show that only when the physicochemical processes underlying morphogenesis and pattern formation are taken into account, would the causal role of development be fully incorporated into the evolutionary view.
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    • "There is an ongoing debate about the roles played by functional and developmental factors and their interactions in influencing morphological variation (Klingenberg , 2005; Hallgr ımsson et al., 2009; Klingenberg et al., 2010). One viewpoint is that genetic modularity should evolve to match developmental and functional modularity (Reidl, 1978; Cheverud, 1982, 1984; Wagner, 1996), whereas more recent studies highlight development as the source of all phenotypic variation (Nemeschal, 1999; Young and Hallgr ımsson, 2005; Zelditch and Swiderski, 2011). According to the latter viewpoint, for genetic (or phenotypic) modularity to match functional modularity, developmental interactions must evolve to match functional interactions. "
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    American Journal of Physical Anthropology 07/2014; 154(3). DOI:10.1002/ajpa.22520 · 2.51 Impact Factor
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    • "In addition, the radius and ulna must interact during pronation and supination movements , which are important during locomotion and other behaviours (such as grasping, digging, prey capture and grooming). Consequently, we predict that there will be a greater degree of shape co-variation and morphological Fig. 2 Schematic representation of the developmental expression of 5 0 Hox paralogous 9–13 involved in the proximodistal patterning of forelimb in mice (modified from Wellik & Capecchi, 2003; Young & Hallgr ımsson, 2005; Schmidt & Fischer, 2009; Young et al. 2010) showing in the first box the developmental modules: the blue box represents the humerus module and the yellow box represents the ulna and radius module; the second box represents functional modules involved in movements of rotation (green) and flexion–extension (red). Primary expression pattern is shown in black; lesser expression is shown in grey. "
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