Inter-individual physiological variation in responses to environmental variation and environmental change: Integrating across traits and time

Abstract

Greater understanding of physiological responses to climate change demands deeper comprehension of the causes and consequences of physiological variation. Increasingly, population trait means are being deconstructed into variable signals at the level of individuals. We advocate for greater consideration of such inter-individual physiological variation and how it both depends on and interacts with environmental variability. First, we review several studies on the intertidal mussel Mytilus californianus to illustrate how the magnitude of inter-individual variation may depend on the environmental context analyzed (i.e., is the mean condition benign or stressful?) and/or on the specific physiological metric investigated. Stressful conditions may reveal or mask variation in disparate ways at different levels of analysis (e.g., transcriptome vs. proteome), but we often lack crucial information regarding the relationships among these different physiological metrics and their consequences for fitness. We then reanalyze several published datasets to ask whether individuals employ divergent strategies over time in response to acute heat stress; such time-dependence would further complicate interpretation of physiological variation. However, definitive conclusions are precluded by limited sample sizes and short timescales in extant datasets. A key remaining challenge is to extend these analytical frameworks to longer periods over which individuals in a population experience repeated, but spatially variable, episodic stress events. We conclude that variation at multiple levels of analysis should be investigated over longer periods and, where possible, within individuals (or genotypes) experiencing repeated environmental challenges. Although difficult in practice, such studies will facilitate improved understanding of potential population-level physiological responses to climate change.