How organisms adapt to changing environments is a question that pervades all biological disciplines and is especially relevant given the pace of global climate change. Hormone concentrations are highly sensitive to environmental variation. In mammalian species, early exposure to hormones can have profound implications on offspring physiology, growth rates, and behavior. The goal of this project is to examine how the hormonal responses of wild red squirrels to environmental variation can adaptively modify offspring due to variable hormone exposure before birth. Red squirrels are an ideal study system to determine the importance of the endocrine system in adapting to changing environments because the survival and future reproduction of offspring can be monitored. The proposed research will integrate ecology, physiology, and evolution to understand the mechanisms by which animals can adapt to changing environments. Broader impacts include furthering our understanding about how organisms living at northern latitudes can respond to global climate change, training undergraduate students in field data collection as well as allowing them to participate in their own independent research projects, and continuing outreach activities with local aboriginal and underrepresented groups in the Yukon, Canada.
In humans, parents make important contributions to their offspring to try and prepare them for the environment that they will encounter at independence. In wild animals, the appropriate preparation of offspring for the outside world can vary dramatically from one year to the next. This project focused on understanding if female red squirrels were able to predict what type of environment their offspring will encounter and prepare them, using early exposure to stress hormones, in such a way to promote their survival in that predicted environment. Over the past 22 years, the survival and reproduction of free-living red squirrels in the Yukon, Canada has been followed. In each year, the amount of food available to red squirrels fluctuates and, accordingly, the population density of squirrels also varies from year to year. Under high-density conditions, only the fastest growing offspring survived. In this study, female red squirrels were tricked into thinking that they were reproducing in a high-density environment using audio playbacks of territorial vocalizations. Females that were tricked into thinking their offspring would encounter a high-density environment produced faster growing offspring, which was surprising given that they did not have access to additional food. The mechanism by which females increased the growth rates of their offspring under high-density conditions was through elevated early exposure to maternal stress hormones. Pregnant females had elevated levels of stress hormones under high-density conditions and those with the highest levels of stress hormones (either naturally or experimentally increased) produced the fastest growing offspring. How these experimental increases in exposure to maternal stress hormones affected the physiology and neuroanatomy is currently being investigated. This research highlights that the social environment can induce changes in the stress hormone levels of pregnant females that results in adaptive changes in offspring characteristics that actually improves the ability of offspring to survive under those anticipated environmental conditions. This research also provides some new insight into understanding how parents can use hormone-mediated maternal effects to prepare their offspring for future or changing environmental conditions. This study also challenges the general assumption that elevated exposure to maternal stress hormones early in life is detrimental for offspring. In this study, free-living female red squirrels with elevated levels of stress hormones during pregnancy produced faster growing offspring, thereby increasing the ability of their offspring to survive in the predicted high-density environment. This research highlights the importance of studying how hormones influence survival and reproduction in wild animals so that we can better understand the evolution of the same mechanisms in humans. Broader impacts of this project included furthering our understanding about how organisms living at northern latitudes can respond to environmental changes, training undergraduate and graduate students from underrepresented groups in field and laboratory data collection as well as allowing them to participate in their own independent research projects, and training graduate students in how to mentor and train undergraduate students in scientific data collection and experimental design.
