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

Genetic variation in functionally integrated skeletal traitscan be maintained over 10 million years despite bottlenecksand stringent selection. Here, we describe an analysis of thegenetic architecture of the canid axial skeleton using populationsof the Portuguese Water Dog Canis familiaris) and silver fox(Vulpes vulpes). Twenty-one skeletal metrics taken from radiographsof the forelimbs and hind limbs of the fox and dog were usedto construct separate anatomical principal component (PC) matricesof the two species. In both species, 15 of the 21 PCs exhibitedsignificant heritability, ranging from 25% to 70%. The secondPC, in both species, represents a trade-off in which limb-bonewidth is inversely correlated with limb-bone length. PC2 accountsfor approximately 15% of the observed skeletal variation, 30%of the variation in shape. Many of the other significant PCsaffect very small amounts of variation (e.g., 0.2–2%)along trade-off axes that partition function between the forelimbsand hind limbs. These PCs represent shape axes in which an increasein size of an element of the forelimb is associated with a decreasein size of an element of the hind limb and vice versa. In mostcases, these trade-offs are heritable in both species and geneticloci have been identified in the Portuguese Water Dog for manyof these. These PCs, present in both the dog and the fox, includeones that affect lengths of the forelimb versus the hind limb,length of the forefoot versus that of the hind foot, musclemoment (i.e., lever) arms of the forelimb versus hind limb,and cortical thickness of the bones of the forelimb versus hindlimb. These inverse relationships suggest that genetic regulationof the axial skeleton results, in part, from the action of genesthat influence suites of functionally integrated traits. Theirpresence in both dogs and foxes suggests that the genes controllingthe regulation of these PCs of the forelimb versus hind limbmay be found in other tetrapod taxa.