Macronutrient composition and availability affects repeatability of fly activity through changes in among- and within-individual (residual) variation

Understanding how environmental conditions affect trait expression in animals is important for estimating the evolutionary potential of that trait. Two different mechanisms have been proposed to explain changes in phenotypic trait variation and heritability across different nutritional environments: (1) selection history, in which trait variance is reduced in environments that match the recent evolutionary history of a population, and (2) nutrient availability, in which trait variance is reduced when there are insufficient resources. Here, we ask which mechanism better explains patterns of repeatability (an upper estimate for heritability) of locomotor activity across a multidimensional nutritional landscape in the Queensland fruit fly (Q-flies). We fed Q-flies one of 15 chemically-defined diets differing in energy density (calories) and composition (protein-to-carbohydrate ratio, P:C), and monitored activity levels continuously. As predicted by the nutrient availability hypothesis, repeatability increased with the carbohydrate content of the diet, mirroring the landscape pattern for mean activity patterns. Thus, our results suggest that nutrient availability (and not selection history) limits expression of genetic variation of activity in Q-flies, and hence is largely responsible for the changing repeatability across different nutritional environments. Our results highlight the importance of considering complexities of both nutrient content and composition in studies of the evolutionary potential of traits, and in studies of individual variation in behaviour that rarely consider complexities of diet quantity and quality in affecting trait expression.