Abstract
Gene expression variation within species is relatively common, however, the role of natural selection in the maintenance of this variation is poorly understood. Here we investigate low and high latitude populations of Drosophila melanogaster and its sister species, D. simulans, to determine whether the two species show similar patterns of population differentiation, consistent with a role for spatially varying selection in maintaining gene expression variation. We compared at two temperatures the whole male transcriptome of D. melanogaster and D. simulans sampled from Panama City (Panama) and Maine (USA). We observed a significant excess of genes exhibiting differential expression in both species, consistent with parallel adaptation to heterogeneous environments. Moreover, the majority of genes showing parallel expression differentiation showed the same direction of differential expression in the two species and the magnitudes of expression differences between high and low latitude populations were correlated across species, further bolstering the conclusion that parallelism for expression phenotypes results from spatially varying selection. However, the species also exhibited important differences in expression phenotypes. For example, the genomic extent of genotype × environment interaction was much more common in D. melanogaster. Highly differentiated SNPs between low and high latitudes were enriched in the 3’ UTRs and CDS of the geographically differently expressed genes in both species, consistent with an important role for cis-acting variants in driving local adaptation for expression-related phenotypes.
Highlights
Parallel adaptive evolution in natural populations has been of longstanding interest to evolutionary biologists because its prevalence speaks to the repeatability of adaptive trajectories or mechanisms and in doing so, informs our understanding of the general “rules” of divergence under selection
We observe substantial parallelism in expression differences and expression plasticity between populations, which supports the idea that spatially varying selection correlated with latitude contributes to the maintenance of gene expression variation in these species
To identify genes that are differentially expressed between low and high latitude populations, we characterized population variation in whole male transcriptomes of D. melanogaster and D. simulans at 21°C and 29°C using sympatric isofemale strains established from flies collected in Maine and Panama
Summary
Parallel adaptive evolution in natural populations has been of longstanding interest to evolutionary biologists because its prevalence speaks to the repeatability of adaptive trajectories or mechanisms and in doing so, informs our understanding of the general “rules” of divergence under selection. Less well understood is whether D. simulans, the sister species of D. melanogaster, shows latitudinal differentiation, and if so, whether there is substantial overlap in the targets of spatially varying selection in the two species. Unlike D. melanogaster, which is polymorphic for a number of clinally varying paracentric chromosome inversions [22,23], D. simulans segregates no common chromosome inversions [24]. Despite this major cytological difference between the two species, their recent shared ancestry and general population genetic similarities suggest the possibility that their evolutionary response to recent colonization of novel habitats might be similar in magnitude and perhaps even overlap substantially in the genetic details. A relatively unbiased and large-scale approach for generating hypotheses regarding the extent and biological basis of parallel latitudinal adaptation in the two species is characterization of gene expression variation
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