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Abstract

Our understanding of the genetic basis of complex traits, including fitness-related traits, is mostly based on mapping studies that identify genotype-to-phenotype associations. Due to the challenges in performing high-resolution mapping experiments, such genotype-phenotype map in usually explored in just one environment. However, evolutionary theory as well as empirical work suggest that such map is often environmentally dependent, and that such genotype-by- environment (GxE) interactions are key to understanding phenotypic variation. Here, we use a large population of outbred Drosophila melanogaster to identify the genetic basis of lifespan in two conditions: control and high sugar diets. We sequenced over 10,000 individual flies to track genome-wide allele frequency changes over the lifetime of six replicate populations, recording in real time the changes in the genomic composition of each population as flies aged. The high statistical power of this experimental design allowed us to draw the genotype- phenotype map for lifespan variation under control conditions, and the way such map got remodeled in response to dietary stress. Remarkably, a third of the lifespan-associated alleles appear cryptic in control diet but play an important role in high sugar conditions. Our results provide strong evidence for the pervasive nature of cryptic genetic variation and the key role that it plays in shaping phenotypic variation between individuals.