Adaptive endocrine and behavioral responses of free-living red squirrels to environmental variation

Free-living animals live in an environment of constant uncertainty and the challenge for them is to adapt to these fluctuating environments. Phenotypic plasticity occurs when the environment induces phenotypic modifications. Maternal effects are a form of transgenerational phenotypic plasticity that may enable females to adjust offspring phenotype adaptively in response to fluctuating environments. My dissertation broadly focused on understanding the endocrine and behavioral responses of free-living North American red squirrels (Tamiasciurus hudsonicus) to variation in population density and whether the endocrine responses of females induced adaptive phenotypic plasticity in offspring phenotype. Red squirrels at my study site in the Yukon, Canada experience pronounced fluctuations in population density. Offspring postnatal growth rates experience density-dependent natural selection such that natural selection favors females that produce the fastest growing offspring in years of high-density, whereas selection relaxed in low-density years. The overarching hypothesis that I tested was that information about the competitive environment (population density) that is acquired during reproduction is used by female red squirrels to adaptively modify offspring phenotype through hormone-mediated maternal effects. To test this hypothesis, I first developed and validated enzyme-immunoassays to measure fecal cortisol metabolite (FCM) and fecal androgen metabolite (FAM) concentrations. Second, in breeding females, I determined that FCM concentrations peaked around parturition whereas FAM concentrations peaked around the period of time when juveniles were first emerging from their natal nest. Third, I found that FAM concentrations in breeding females tended to co-vary with major changes in maternal behavior. Fourth, I found that slight differences in the diets of red squirrels could induce profound effects on FCM and FAM concentrations. Fifth, I found that under naturally or experimentally heightened population density, both male and females spent less time in their nest and feeding, but more time being vigilant. Under high population density, squirrels emitted significantly more territorial vocalizations but there was either no or a negative relationship between population density and the frequency of physical interactions. Finally, I found that female red squirrels adaptively increased offspring postnatal growth rates in response to the perception of increased competitive density. Breeding females experiencing naturally or experimentally heightened density, as well as those experiencing heightened perceived density, had higher FCM and FAM concentrations than females experiencing lower density conditions. These endocrine responses to population density induced adaptive maternal effects on offspring growth rates, as I found that heightened FCM and FAM concentrations synergistically elevated offspring postnatal growth rates. This suggests that the endocrine responses of breeding females to perceived competitive intensity induced an adaptive endocrine-mediated maternal effect on offspring phenotype. Overall, my dissertation elucidates how maternal effects can induce adaptive phenotypic plasticity in offspring phenotype to facilitate adaptation to fluctuating environments as well as some of the endocrine mechanisms mediating these maternal effects.