Pervasive fitness trade-offs revealed by rapid adaptation in large experimental populations of Drosophila melanogaster

Life-history trade-offs are an inherent feature of organismal biology that evolutionary theory posits play a key role in patterns of divergence within and between species. Efforts to quantify trade-offs are largely confined to phenotypic measurements and the identification of negative genetic-correlations among fitness-relevant traits. Here, we use time-series genomic data collected during experimental evolution in large, genetically diverse populations of Drosophila melanogaster to directly measure the manifestation of trade-offs in response to temporally fluctuating selection pressures on ecological timescales. Specifically, we quantify the genome-wide signal of antagonistic pleiotropy suggestive of trade-offs between reproduction and stress tolerance. We further identify a putative role of two cosmopolitan inversions in these trade-offs, and show that loci responding to selection during lab-based, reproduction selection exhibit signals of fluctuating selection in an outdoor mesocosm exposed to natural environmental conditions. Our results demonstrate the utility of time-series genomic data in revealing the presence and genomic architecture underlying fitness trade-offs, and add credence to models positing a role of generic life history trade-offs in the maintenance of variation in natural populations.