Genome-wide selection signatures reveal widespread synergistic effects of two different stressors in Drosophila melanogaster

Experimental evolution combined with whole-genome sequencing (E&R) is a powerful approach to study the adaptive architecture of selected traits. Nevertheless, so far the focus has been on the selective response triggered by a single stressor. Building on the highly parallel selection response of founder populations with reduced variation, we evaluated how the presence of a second stressor affects the genomic selection response. After 20 generations of adaptation to laboratory conditions at either 18°C or 29°C, strong genome-wide selection signatures were observed and almost the entire genome was affected by selection. Only about one third of the selection signatures can be attributed to laboratory adaptation (no difference between temperature regimes). The remaining selection responses are either caused by temperature specific effects, or reflect the joint effects of temperature and laboratory adaptation (same direction, but the magnitude differs between temperatures). The allele frequency changes resulting from the combined effects of temperature and laboratory adaptation were more extreme in the hot environment for 83% of the affected genomic regions – indicating widespread synergistic effects of the two stressors. We conclude that E&R with reduced genetic variation is a powerful approach to study genome-wide fitness consequences driven by the interaction of multiple environmental factors. Furthermore, laboratory adaptation can have a major impact on the selection response and E&R studies contrasting ancestral and evolved populations can easily confound laboratory adaptation with a response to the focal trait.