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

Eugenia Rashkovetsky,Eviatar Nevo,Lin Kang,Abraham Korol,Pawel Michalak,Katarzyna Michalak,Harold R Garner,James E Mahaney,Beverly A Rzigalinski

doi:10.1073/pnas.1720938116

Abstract

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.

Highlights

Climate variation and change are major abiotic stresses driving life’s evolution [1,2,3]
Genome pool-sequencing of 18 D. simulans isofemale lines resulted in 73× coverage and an average mapping rate of 99.26% (SI Appendix, Table S1)
We found a total of 4,564,564 single nucleotide polymorphism (SNP) sites, including 9% synonymous substitutions and 4% were nonsynonymous substitutions (SI Appendix, Table S2)

Summary

Introduction

Climate variation and change are major abiotic stresses driving life’s evolution [1,2,3]. Significant insights can be provided by local adaptations emerging across thermal gradients These gradients are perhaps most dramatic in the Mediterranean region proper, where arid slope landforms produce local biodiversity refugia with microclimate contrasts of a magnitude equivalent to a multiyear temperature increase under rapid climatic change [15,16,17]. One such site in particular, known as Evolution Canyon (Lower Nahal Oren, Mount Carmel, Israel), has long served as a natural system in which convergent local adaptations are observed in many taxa inhabiting this ecological microgradient [18,19,20,21]. 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

Methods

Results

Discussion

Conclusion