Genomic divergence and adaptive convergence in Drosophila simulans from Evolution Canyon, Israel

Abstract

Significance Adaptation to temperature and drought stress in Drosophila can be experimentally explored as a proxy model for adaptive trait complexes and genomic responses to climate variation. As a snapshot of synchronized adaptive events in a climate gradient, contemporary convergent evolution empowers the detection and understanding of adaptation from population genomic data and advance climate change assessment and forecasting. However, the effects of climate change on living organisms have been shown primarily on regional and global scales, confounding climate-related and climate-unrelated multivariate factors. This study leverages a unique microclimate contrast, known as Evolution Canyon, and a Drosophila model within it to provide a whole-genome perspective of adaptive evolution, convergence under thermal stress, and incipient speciation. Biodiversity refugia formed by unique features of the Mediterranean arid landscape, such as the dramatic ecological contrast of “Evolution Canyon,” provide a natural laboratory in which local adaptations to divergent microclimate conditions can be investigated. Significant insights have been provided by studies of Drosophila melanogaster diversifying along the thermal gradient in Evolution Canyon, but a comparative framework to survey adaptive convergence across sister species at the site has been lacking. To fill this void, we present an analysis of genomic polymorphism and evolutionary divergence of Drosophila simulans, a close relative of Drosophila melanogaster with which it co-occurs on both slopes of the canyon. Our results show even deeper interslope divergence in D. simulans than in D. melanogaster, with extensive signatures of selective sweeps present in flies from both slopes but enhanced in the population from the hotter and drier south-facing slope. Interslope divergence was enriched for genes related to electrochemical balance and transmembrane transport, likely in response to increased selection for dehydration resistance on the hotter slope. Both species shared genomic regions that underwent major selective sweeps, but the overall level of adaptive convergence was low, demonstrating no shortage of alternative genomic solutions to cope with the challenges of the microclimate contrast. Mobile elements were a major source of genetic polymorphism and divergence, affecting all parts of the genome, including coding sequences of mating behavior-related genes.