The evolutionary importance of maternal effects is determined by the interplay of maternal adaptations and strategies, offspring susceptibility to these strategies, and the similarity of selection pressures between the two generations. Interaction among these components, especially in species where males and females differ in the costs and requirements of growth, limits inference about the evolution of maternal strategies from their expression in the offspring phenotype alone. As an alternative approach, we examine divergence in the proximate mechanisms underlying maternal effects across three house finch populations with contrasting patterns of sex allocation: an ancestral population that shows no sex-biased ovulation, and two recently established populations at the northern and southern boundaries of the species range that have opposite sequences of ovulation of male and female eggs. For each population, we examined how oocyte acquisition of hormones, carotenoids and vitamins was affected by oocyte growth and overlap with the same and opposite sexes. Our results suggest that sex-specific acquisition of maternal resources and sex determination of oocytes are linked in this system. We report that acquisition of testosterone by oocytes that become males was not related to growth duration, but instead covaried with temporal exposure to steroids and overlap with other male oocytes. In female oocytes, testosterone acquisition increased with the duration of growth and overlap with male oocytes, but decreased with overlap with female oocytes. By contrast, acquisition of carotenoids and vitamins was mostly determined by organism-wide partitioning among oocytes and oocyte-specific patterns of testosterone accumulation, and these effects did not differ between the sexes. These results provide important insights into three unresolved phenomena in the evolution of maternal effects - (i) the evolution of sex-specific maternal allocation in species with simultaneously developing neonates of both sexes; (ii) the link between sex determination and sex-specific acquisition of maternal products; and (iii) the evolution of context-dependent modulation of maternal effects.
Species that depend on ephemeral habitat often evolve distinct dispersal strategies in which the propensity to disperse is closely integrated with a suite of morphological, behavioural and physiological traits that influence colonizing ability. These strategies are maintained by natural selection resulting from spatial and temporal variation in resource abundance and are particularly evident during range expansion. Yet the mechanisms that maintain close alignment of such strategies with resource availability, integrate suites of dispersal traits and generate variability in dispersal propensity are rarely known. Breeding females can influence offspring phenotype in response to changes in current environmental conditions, making maternal effects uniquely suited to bridge fluctuations in resource abundance in the maternal generation and variation in offspring dispersal ability. Western bluebirds' (Sialia mexicana) dependence on nest cavities--an ephemeral resource--has led to the evolution of two distinct dispersal phenotypes: aggressive males that disperse and non-aggressive males that remain philopatric and cooperate with their relatives. Over the last 40 years, western bluebirds rapidly expanded their geographical range, providing us with an opportunity to test, in newly established populations, the importance of maternal effects for generating variability in dispersal propensity. Here, I show that, under variable resource conditions, breeding females group offspring of different competitive ability in different positions in the egg-laying order and, consequently, produce aggressive males that are more likely to disperse when resources are low and non-aggressive philopatric males when resources are abundant. I then show experimentally that the association between resource availability and sex-specific birth order is robust across populations. Thus, this maternal effect enables close tracking of resource availability and may explain how variation in dispersal is generated in newly colonized populations. More generally, these results suggest that, as a key source of variation in colonizing phenotypes, maternal effects are of crucial importance for understanding the dynamics of range expansion.
