Phylogenetic Relatedness Does not Predict Patterns of Parallel Transcriptome Adaptation in Drosophila

Identifying the factors determining the repeatability of adaptation is a long-standing problem in evolutionary biology. Addressing this problem requires both comparative analysis and an understanding of how genetic variation within species responds to natural selection. Latitudinal clines are a classic system for studying adaptation in many species, including Drosophila. Here we investigate male reproductive tract (testis and accessory gland [AG]) transcriptomes from Maine (USA) and Panama City (Panama) populations of three species that have recently colonized North America, a pair of close relatives, Drosophila melanogaster, Drosophila simulans, and a much more distantly related species, Drosophila hydei. We observed strong evidence of parallel gene expression adaptation in the AG, but little such evidence for the testis. This parallelism takes the form of genes that exhibit high vs. low latitude expression differentiation in multiple species, as well as between-species correlations of high vs. low latitude log fold changes. However, the degree of parallelism among these species is not related to their relatedness. More specifically, D. simulans, which is very closely related to D. melanogaster yet very distantly related to D. hydei, shows much stronger parallelism for latitudinal AG transcriptome differentiation with the latter than with the former. This, despite the reproductive biology of D. melanogaster and D. simulans, is very similar and highly diverged from that of D. hydei. These results suggest that despite a signal of adaptive parallelism among all three species, the underlying selection responses are not well predicted by relatedness or similar ecologies, suggestive of idiosyncratic processes operating simultaneously with deterministic ones.