Abstract
Whether hard sweeps or soft sweeps dominate adaptation has been a matter of much debate. Recently, we developed haplotype homozygosity statistics that (i) can detect both hard and soft sweeps with similar power and (ii) can classify the detected sweeps as hard or soft. The application of our method to population genomic data from a natural population of Drosophila melanogaster (DGRP) allowed us to rediscover three known cases of adaptation at the loci Ace, Cyp6g1, and CHKov1 known to be driven by soft sweeps, and detected additional candidate loci for recent and strong sweeps. Surprisingly, all of the top 50 candidates showed patterns much more consistent with soft rather than hard sweeps. Recently, Harris et al. 2018 criticized this work, suggesting that all the candidate loci detected by our haplotype statistics, including the positive controls, are unlikely to be sweeps at all and that instead these haplotype patterns can be more easily explained by complex neutral demographic models. They also claim that these neutral non-sweeps are likely to be hard instead of soft sweeps. Here, we reanalyze the DGRP data using a range of complex admixture demographic models and reconfirm our original published results suggesting that the majority of recent and strong sweeps in D. melanogaster are first likely to be true sweeps, and second, that they do appear to be soft. Furthermore, we discuss ways to take this work forward given that most demographic models employed in such analyses are necessarily too simple to capture the full demographic complexity, while more realistic models are unlikely to be inferred correctly because they require a large number of free parameters.
Highlights
Pervasive adaptation has been extensively documented in Drosophila melanogaster
We proposed novel statistics that can identify and differentiate hard and soft sweeps and found that soft sweeps are surprisingly common in North American Drosophila melanogaster
Harris et al 2018 have claimed that the selective sweeps we identified are false positives and are more likely to be explained by an admixture demographic history
Summary
Pervasive adaptation has been extensively documented in Drosophila melanogaster. Recent studies suggest that (i) ~50% of amino acid changing and non-coding substitutions in D. melanogaster evolution were adaptive, and (ii) there are abundant signatures of adaptation in the population genomic data detectable as reductions of neutral diversity in the regions of higher functional divergence and as elevation in the frequencies of derived alleles above neutral expectations [1,2,3,4,5,6,7,8,9,10,11].In three cases—at the loci CYP6g1, CHKov, and Ace–we know the causal mutations and have functional hypotheses for the causes of adaptation [12,13,14,15,16,17,18]. At the CHKov locus, the adaptive change led to a higher resistance to organophosphates and viral infections and evolved by a transposon element insertion in the protein coding region of CHKov, which segregated in the ancestral populations before rising to high frequency only recently [14,15]. All three well-understood examples of adaptation are, by definition, known soft sweeps (Fig 1) in which multiple adaptive alleles have risen to high frequency simultaneously at the same locus [19,20,21]. This suggests that recent and strong adaptation is not mutation-limited in D. melanogaster [16]
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