We have demonstrated the existence of DA in the several skeletal systems of the silver fox. Left-right asymmetric values were obtained for the limb bones, the mandibles and both the ileum and ischium in the pelvic girdle. Because of the size of the populations analyzed, we were able to establish significant asymmetries involving small differences between left and right metrics. Our data demonstrate that skeletal metrics in the fox populations vary around mean values that differ for each metric. For some metrics, the mean value is greater on the left than on the right, for others greater on the right than on the left. Hence, we observe DA.
We analyzed foxes from different populations, as well as progeny from crosses between these populations. These populations had been shown to be genetically different and progeny developed from crosses between these populations display heritable variation in skeletal morphology (Kharlamova et al., 2007
). Nevertheless, we were unable to demonstrate heritable variation in skeletal DA. Variation around these values can be due to a number of environmental effects, which may obscure minor differences in the DA values. If so, the genetic signal must be smaller than 25% which is the limit of our power to detect heritability in this population. (In the mouse, Leamy et al. (2000
) found that heritable variation of mandibular DA was very low, well below our limit of detection.) Alternatively, the failure to detect segregation of DA would be expected if values of DA were genetically fixed in the fox (see discussion below).
Not surprisingly, the magnitudes of asymmetry of the radius and ulna were highly correlated. There also was significant correlation between the asymmetric properties of the humerus and those of the radius and ulna (). These correlations extended to the olecranon and elbow joint. Thus, at some level, the asymmetries in growth of the forelimb appear to be coordinated. However, no such correlation (or inverse correlation) could be found for the magnitude of the inverse DA vectors for the length and width metrics of the limb bones, the ileum and ischium, or of the mandible.
The consistent inverse directional relationship between length and width is in striking contrast to observations of DA in porpoise (Galatius, 2005
), human (Kujanová et al., 2008
), or macaque (Falk et al., 1988
), in which lengths and widths of the bones of the forelimb have the same DA vector (R > L except for the radius of the macaque in which length and width are both L > R). In all of those cases, it was argued that DA derived from a behavioral bias that resulted in greater usage of the directionally favored limb (handedness). We tested for behavioral bias by presenting foxes with the need to rotate food containers into their cage, which they could do using either the right or left forelimb. Although there were significant preferences by individual foxes to use either the right or the left forelimb, the population was not heavily biased toward one side or the other (i.e., this behavior presents as fluctuating rather than DA). Although there may be a behavioral bias that affects the directional asymmetries described here, we have not observed such behavior. Because movement of these animals is restricted within their cage behavioral differences may have less of an impact on skeletal loading. However, the consistent inverse vectorial relationship of length to width observed in the skull, and pelvis as well as the limb bones is difficult to attribute to a behavioral bias. Moreover, any such behavioral explanation would have to account for the inverse vectorial DA of the ileum and ischium.
We would like to propose an alternative to behavior as a basis for the observed directional asymmetries: The most important component of canine skeletal shape (other than size) is the inverse correlation between length and width of various bones observed in both foxes and dogs (Carrier et al., 2005
; Kharlamova et al., 2007
). This inverse relationship is heritable and in dogs, genetic loci regulating this variation have been identified (Carrier et al., 2005
; Lark et al., 2006
; Parker et al., 2009
; Quignon et al., 2009
). Previous results analyzing the pelvis of the dog (C. familiaris
) have demonstrated a shape component in which the lengths of the ilium and ischium also were inversely correlated. That relationship was heritable and loci regulating that relationship also were identified (see Fig. 2 in Carrier et al., 2005
Here, we have seen a striking similarity that governs the vectorial relationship of the asymmetries of the limbs, skull, and pelvis whereby the DA vector of length is always opposite to that of width. This inverse vectorial relationship of length/width DA may be related to the inverse relationship between overall length and width observed in previous studies. For example, if growth on the right and left sides of the animal are differentially biased, such that one either terminates slightly ahead or after the other, then a longer bone would necessarily also be thinner (because of the inverse relationship between overall length and width), giving rise to opposing asymmetries for length and width. Lack of correlation in the amount of asymmetric growth (length vs. width) would represent random variation (noise) in the growth process (e.g., in the supply of nutrients to the tissues during growth). The results in , comparing asymmetries during postnatal growth, suggest that such inequalities between growth rates (or of periods of growth) on the left and right sides change in magnitude and direction with age, a result previously observed in macaques (Helmkamp and Falk, 1990
This concept of differential bilateral skeletal growth is supported by genetic evidence that in dogs, the laxity of the right coxofemoral joint is regulated by one locus whereas the left is regulated by another (Chase et al., 2004
; Todhunter et al., 2005
). A similar explanation of vectorial asymmetries could apply to the ilium and ischium, i.e., as a result of regulation of growth of the ilium and ischium, when the illium was longer the ischium would necessarily be shorter and as a consequence, asymmetries of the two would be reversed.
In summary, our data suggest that for the majority of skeletal growth parameters, growth on the right and left side of the fox may be differentially biased, resulting in fixed differences between the two sides in either the rate of growth or the length of the period during which growth occurs, giving rise to DA. Random effects around these fixed differences (i.e., noise) perturb the magnitude of the effects such that length and width asymmetries are not inversely correlated at the level of individual animals.