Genomics of parallel adaptation at two timescales in Drosophila

Abstract

Two interesting unanswered questions are the extent to which both the broad patterns and genetic details of adaptive divergence are repeatable across species, and the timescales over which parallel adaptation may be observed. Drosophila melanogaster is a key model system for population and evolutionary genomics. Findings from genetics and genomics suggest that recent adaptation to latitudinal environmental variation (on the timescale of hundreds or thousands of years) associated with Out-of-Africa colonization plays an important role in maintaining biological variation in the species. Additionally, studies of interspecific differences between D. melanogaster and its sister species D. simulans have revealed that a substantial proportion of proteins and amino acid residues exhibit adaptive divergence on a roughly few million years long timescale. Here we use population genomic approaches to attack the problem of parallelism between D. melanogaster and a highly diverged conger, D. hydei, on two timescales. D. hydei, a member of the repleta group of Drosophila, is similar to D. melanogaster, in that it too appears to be a recently cosmopolitan species and recent colonizer of high latitude environments. We observed parallelism both for genes exhibiting latitudinal allele frequency differentiation within species and for genes exhibiting recurrent adaptive protein divergence between species. Greater parallelism was observed for long-term adaptive protein evolution and this parallelism includes not only the specific genes/proteins that exhibit adaptive evolution, but extends even to the magnitudes of the selective effects on interspecific protein differences. Thus, despite the roughly 50 million years of time separating D. melanogaster and D. hydei, and despite their considerably divergent biology, they exhibit substantial parallelism, suggesting the existence of a fundamental predictability of adaptive evolution in the genus.

Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

“…First, a high level of genetic diversity in the species provides substantial standing genetic variation and potentially beneficial mutations. Similarly, Zhao et al [49] showed that the more genetically diverse species Drosophila hydei contained more adaptive alleles than D. melanogaster. Second, the recent timing of expansion and divergence in maize has likely affected the extent of parallelism.…”

The genomic basis of environmental adaptation in house mice

“…In recognition of this, a second widely adopted approach is to generate an empirical distribution of a given summary statistic and to compare individual loci to the genome-wide distribution under the assumption that loci subject to selection will be outliers [e.g. 78 – 84 ]. The rationale for this approach is that the demographic history of the population will shape patterns of variation genome-wide, so that the distribution of variation across loci will reflect the demographic history even if the actual history is unknown.…”

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

“…The recent development of genomics has allowed identification of clinal genomic variants, which are candidates for thermal adaptation (e.g., Kolaczkowski et al 2011; Fabian et al 2012; Bozicevic et al 2016; Mateo et al 2018). There is also evidence of parallel evolution at the genomic and transcriptomic level (Reinhardt et al 2014; Bergland et al 2015; Machado et al 2015; Zhao et al 2015; Juneja et al 2016; Zhao and Begun 2017). Some of these studies compared clines between species (which may have somewhat distinct biology), while others compared clines between Australia and North America (which both feature primarily European ancestry with clinally variable African admixture).…”