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Intragenic epistasis in couch potato and its effect on climatic adaptation in natural populations

Epistatic variance for fitness-related traits can fundamentally affect the efficacy of natural selection and adaptation in the wild; however, the extent of non-additivity among alleles in natural populations is generally unknown. Previous mapping in Drosophila melanogaster has identified that the couch potato gene (cpo) is involved with climatic adaptation by controlling the propensity of a reproductive diapause associated with overwintering in temperate climates. A screen of wild populations of Drosophila sampled across spatial and temporal scales identified three novel SNPs in cpo that vary predictably with climate in independent clines; however, certain multi-SNP combinations vary non-randomly with geographic location. This suggests that epistatic interactions among independent SNPs in cpo influence organismal performance and fitness-related traits that underlie adaptation to climate. Here, this hypothesis is tested using DGRP inbred lines to create populations that are constant for one of the three-SNP allelic combinations. The performance and fitness of these multi-locus alleles was assessed using a comprehensive phenotypic screen, showing significant variation for all traits investigated and pervasive epistasis among SNPs for these traits. There are emergent properties associated with combinations of SNPs; the northern allelic combination, as defined by the three SNPs whose allele frequency increases with latitude, is characterized by non-additive increases in traits associated with higher fitness in northern environments (e.g., cold tolerance). In contrast, the southern three SNP allelic combination exhibits non-additive increases in traits associated with southern environments (e.g., fecundity). The changes in life history phenotypes correspond with differential gene expression patterns among the allelic combinations. This demonstrates that emergent properties of SNP combinations underlie adaptive life history evolution in natural populations of Drosophila.