Indirect genetic effects in a sex-limited trait: the case of breeding time in red-billed gulls

Female reproductive performance can be strongly affected by male care, so that breeding time, a trait expressed only by females, can be seen as one trait determined by both male and female genotypes. Animal model analyses of a 46-year study of red-billed gulls (Larus novaehollandiae scopulinus) revealed that laying date was not heritable in females (h2 = 0.001 +/- 0.030), but significantly so in males (h2 = 0.134 +/- 0.029). Heritability of breeding time in males probably reflects genetic variability in some other trait such as courtship feeding ability. In line with predictions of evolutionary models incorporating indirect genetic effects, the strong and consistent directional selection for advanced breeding time has not resulted in detectable selection response in males. Our results demonstrate that a female trait is largely determined by genetic characteristics of its mate, and hence, any evolutionary change in red-billed gull breeding time depends critically on genetic variation in males.