Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins

Overlap in growth of offspring should constrain the opportunity for sex-biased maternal effects, yet sex-specific allocation of maternal resources among simultaneously growing ova is often observed in vertebrates. In birds, such allocation can be accomplished either by temporal clustering of ova that become the same sex, resulting in sex-biased egg-laying order, or by follicle-specific delivery of maternal resources. Two house finch populations at the northern and southern boundaries of the species range have opposite ovulation sequences of male and female eggs, and thus, in the absence of sex differences in ova growth or sex-specific maternal strategies, would be expected to have opposite sex-specific accumulation of maternal products. We found that the populations had strong and similar gradients of steroid distribution in relation to ovulation order, whereas distribution of carotenoids and vitamins correlated with each follicle's accumulation of steroids. In both populations, temporal bias in production of sons and daughters within a clutch enabled strongly sex-specific acquisition of maternal products, and oocytes of the same sex were highly interdependent in their accumulation of steroids. Moreover, in nests where the sex-bias in relation to ovulation order deviated from population-specific patterns, eggs had highly distinct concentrations of steroids, carotenoids and vitamins. These results and previous findings of sex-specific yolk partitioning among oocytes suggest that oocytes that become males and females are temporally or spatially clustered during their ovarian growth. We discuss the implication of these findings for the evolution of sex-specific maternal resource allocation.