A B S T R A C TDevelopmental plasticity is a widespread property of living organisms, but different individuals in the same species can vary greatly in how susceptible they are to environmental influences. In humans, research has sought to link variation in plasticity to physiological traits such as stress reactivity, exposure to prenatal stress-related hormones such as cortisol, and specific genes involved in major neurobiological pathways. However, the determinants of individual differences in plasticity are still poorly understood. Here we present the novel hypothesis that, in both sexes, higher exposure to androgens during prenatal and early postnatal life should lead to increased plasticity in traits that display greater male variability (i.e., a majority of physical and behavioral traits). First, we review evidence of greater phenotypic variation and higher susceptibility to environmental factors in males; we then consider evolutionary models that explain greater male variability and plasticity as a result of sexual selection. These empirical and theoretical strands converge on the hypothesis that androgens may promote developmental plasticity, at least for traits that show greater male variability. We discuss a number of potential mechanisms that may mediate this effect (including upregulation of neural plasticity), and address the question of whether androgen-induced plasticity is likely to be adaptive or maladaptive. We conclude by offering suggestions for future studies in this area, and considering some research designs that could be used to empirically test our hypothesis.
BackgroundThe social environment that mothers experience during pregnancy and lactation has a strong effect on the developing offspring. Whether offspring can be adaptively shaped to match an environment that is similar to the maternal one is still a major question in research. Our previous work in wild cavies showed that females whose mothers lived in a stable social environment with few social challenges during pregnancy and lactation (SE-daughters) developed different behavioral phenotypes than females whose mothers lived in an unstable social environment with frequent social challenges during pregnancy and lactation (UE-daughters). In the present study we investigated whether SE-daughters are better adapted to a stable social environment, similar to their maternal one, than are UE-daughters, for which the stable social environment represents a mismatch with their maternal one. For this purpose, we established pairs of one UE- and one SE-daughter and housed them together under stable social conditions for one week. Dominance ranks, behavioral profiles, glucocorticoid levels, cortisol responsiveness and body weight changes were compared between the groups. We hypothesized that SE-daughters fare better in a stable social setting compared to UE-daughters.ResultsAfter one week of cohabitation in the stable social condition, UE-daughters had higher glucocorticoid levels, tended to gain less body weight within the first three days and displayed higher frequencies of energy-demanding behaviors such as rearing and digging than SE-daughters. However, there was no difference in cortisol responsiveness as well as in dominance ranks between UE- and SE-daughters.ConclusionHigher glucocorticoid levels and less body weight gain imply that UE-daughters had higher energy demands than SE-daughters. This high energy demand of UE-daughters is further indicated by the increased display of rearing and digging behavior. Rearing implies increased vigilance, which is far too energy demanding in a stable social condition but may confer an advantage in an unstable social environment. Hence, SE-daughters seem to better match a stable social environment, similar to their maternal one, than do UE-daughters, who encountered a mismatch to their maternal environment. This data supports the environmental matching hypothesis, stating that individuals manage the best in environments that correspond to their maternal ones.
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