Recent and strong adaptation in Drosophila melanogaster is driven primarily by soft selective sweeps. Nandita Garud, Philipp Messer, Erkan Buzbas, Dmitri Petrov. Stanford University, Stanford, CA.
Adaptation is typically thought to proceed by the rapid increase in frequency and ultimate fixation of a single adaptive allele. This process results in the signature of a hard sweep, specified by the presence of one haplotype bearing the adaptive allele at high frequency in the population. However, not all modes of adaptation necessarily lead to the presence of a single common haplotype. For instance, in some cases, adaptation might involve subtle changes in frequency at a large number of sites, leaving no signatures of selective sweeps. In other cases, adaptation might drive multiple haplotypes to high frequency, generating signatures of soft sweeps. Such soft sweeps can occur when adaptation involves standing genetic variation, where the adaptive allele was already present in the population prior to the onset of positive selection, or when multiple de novo adaptive mutations arise in the population independently on different haplotypes and sweep through the population simultaneously. Here we developed a haplotype statistic (H12) that identifies both hard and soft sweeps with similar power. We further developed a second statistic (H2/H1) that can determine whether a given sweep identified with H12 was hard or soft. We used these statistics to carry out a genome scan for adaptation in the North Carolina population of D. melanogaster sequenced by DGRP. We found evidence of pervasive haplotype structure suggestive of abundant, recent, and strong adaptation in this population. Interestingly, when we applied our H2/H1 statistic to the 50 most prominent peaks in the scan, we were able to reject the hard sweep hypothesis in every case. On the other hand, the vast majority of the peaks are compatible with a simple model of soft sweeps from multiple de novo mutations. We conclude that recent adaptation in North American populations of D. melanogaster has led primarily to soft sweeps either because it utilized standing variation or because short-term effective population sizes are on the order of billions or larger rather than on the order of millions, as suggested previously.