Epigenetics and adaptive evolution within the family environment

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Parents influence the developmental trajectories of their offspring in many ways beyond the transmission of DNA. In humans, parental life-histories (e.g., diet) and not genetics are significant predictors for the development of various heritable health risks (e.g., diabetes, obesity). Moreover, these disease risks have increased in frequency an order of magnitude within a few decades. These processes are thought to reflect a small snapshot of the larger adaptive evolutionary process. Indeed, parental effects may have consequences on an evolutionary time-scale, buffering or facilitating a population's response to rapid environmental change. Yet classical genetic models of evolution inadequately explain how rapidly traits adapt and change in response to changing environments. One theoretical explanation is that family environments can accelerate these processes. However, the biological mechanisms through which parents may drive adaptive evolutionary change has yet to be elucidated. My project will explore the idea that epigenetic mechanisms might be mediating this process. Epigenetic mechanisms are the biochemical marks and signals that ultimately determine how accessible DNA is to factors within the cell that allow it to be expressed. I have previously shown that these epigenetic factors are induced by changes in the parental and social family environment and can be inherited by offspring from their parents. I propose to examine whether epigenetic mechanisms can also drive adaptive evolutionary change using the burying beetle (Nicrophorus vespilloides) as a model system. This species has a rich and complex social family life but a short lifespan, making rigorous evolutionary epigenetic studies over the course of many generations (e.g., 25+) in this system tractable and feasible.My collaborators have exploited natural variation in care in the burying beetle to establish two types of experimentally evolving populations in the laboratory, which vary only in the family environment that larvae experience during development, and in which the same family environment is created for successive generations within populations. In Full Care populations (FC), parents remain with their young throughout development. In contrast, in No Care populations (NC), parents are removed just before their offspring hatch. This manipulation has revealed that burying beetles are highly responsive to the family environment, and removal of care induces rapid evolutionary change in morphology and behaviour. For example, larvae evolving under NC become more competitive for resources and develop larger mandibles relative to their body size; these traits are correlated with increased larval survival over generations. I plan to investigate the role of epigenetic mechanisms in driving these adaptive evolutionary changes by combining analyses of epigenetic and genetic variation with detailed analyses of parental effects in the egg. This study will be the first to experimentally determine whether epigenetic mechanisms enable the family environment to influence adaptive evolutionary change. Understanding the interaction between genetic and epigenetic change under changing environments and the degree of flexibility afforded by these systems has broad implications for the study of how traits become heritable between generations with applications for the fields of behavioural ecology, conservation, medicine and epidemiology.