Genetic regulation of canine skeletal traits: trade-offs between the hind limbs and forelimbs in the fox and dog

Recent advances in computational tools for quantitative genetics have allowed the genetic analysis of complex, polygenic morphological traits (Barton and Keightly 2002; Doerge 2002; Glazierm et al. 2002; Darvasi 2005). We used these tools in conjunction with molecular genotyping to analyze the genetic basis of variation in the canine skeleton (Chase et al. 2002, 2004; Carrier et al. 2005; Trut et al. 2006; Lark et al. 2006a, 2006b). The dog, Canis familiaris, is one of the most morphologically diverse mammals (Hart 1995; Coppinger and Coppinger 2001; Young and Bannasch 2006). Sizes range from 2 kg (Chihuahua) to 80 kg (Bull Mastiff) and shapes can vary from Basset Hounds and Boxers to Greyhounds and Great Danes. Previously, we analyzed independent combinatorial aspects of skeletal variation using principal component (PC) analysis (Chase et al. 2002; Carrier et al. 2005). PCs vary in a quantitative manner and can be subjected to genetic analysis. PC analysis reduces correlated sets of traits to independent (orthogonal) vectorial components, each of which can be characterized by the projection of the vector onto each of the traits (Venables and Ripley 2002). These “loadings” present the extent and direction (+ or −) of the trait’s contribution to the resulting vector. In previous publications, we used this approach to identify variation in heritable constellations of canine skeletal traits (reviewed by Lark et al. 2006a). A surprising result of this analysis was the discovery that removal of the covariation involved in size (PC1) revealed variation in independent components of shape, suites of functionally integrated traits, each of which were controlled by genetic loci. Quantitative trait loci (QTLs) are regions of the genome that contain one or more genes that regulate PC variation (Darvasi 2005). Thus, genetic analysis of the Portuguese Water Dog led to identification of QTLs responsible for variation in shape defined by canine skeletal PCs composed of groups of functionally related traits. Each of these groupings appeared to vary along a trade-off axis forming a functional compromise between high production of force (as exemplified by the Pit Bull) and energy-efficient speed (as exemplified by the Greyhound). Examples include trade-offs between the skull and postcranial skeleton (Chase et al. 2002) as well as changes in the pelvis and limb bones (Carrier et al. 2005). Using phenotypic data derived from radiograms and polymorphic molecular markers (Simple Sequence Repeats or SSRs), we identified QTLs for these trade-offs. Data from foxes indicated that these trade-offs were ancient and could be identified in the silver fox (Vulpes vulpes), the silver color phase of the red fox, and a member of the outgroup species for the evolutionary lineages of modern canids that separated from C. familiaris 10 million years ago (Wayne 1993; Bardeleben et al. 2005). Here we compare PCs derived from metrics of the forelimbs and hind limbs of Portuguese Water Dogs and silver foxes. We show that both species exhibit similar constellations of traits that affect very small amounts of variation along trade-off axes that partition function between the forelimbs and hind limbs. In most cases, these trade-offs though small in magnitude are heritable in both species and genetic loci regulating these trade-offs have been identified in the Portuguese Water Dog.