The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage

A novel pedigree design is derived that permits separate estimation of X-linked, dominance and maternal effects of sex-linkage and it is suggested that the data from such a design would be most appropriately analyzed using the animal model.

Abstract

Sexual dimorphism (SD) is a defining feature of gonochorous animals and dioecious plants, but the evolution of SD from an initially monomorphic genome presents a conundrum. Theory predicts that the evolution of SD will be facilitated if genes with sex-specific fitness effects occur on sex chromosomes. We review this theory and show that it generates three testable predictions. For organisms with an XX/XY chromosomal system of sex determination: (1) SD should be associated with X-linked effects; (2) X-linked effects should show strong directional dominance for sexually dimorphic traits favored in males but expressed in both sexes; and (3) SD should be associated with a reduction in the between-sex additive genetic covariance and correlation. A literature review reveals that empirical evaluations of the association between sex-linkage and SD have lagged behind theory. Tests for the presence of sex-linked effects have been plagued by the need to make simplifying assumptions, such as the absence of dominance or maternal effects, that greatly weaken their discriminatory power. Further, most have used comparisons between species or populations, whereas the correct level of analysis is within populations. To overcome these problems, we derive a novel pedigree design that permits separate estimation of X-linked, dominance and maternal effects. We suggest that the data from such a design would be most appropriately analyzed using the animal model. This novel protocol will allow quantitative evaluation of the above predictions, and hence should spur progress in understanding the role of sex-linkage in the evolution of SD.