Recent selective sweeps in North American Drosophila melanogaster show signatures of soft sweeps

TL;DR

This study introduces a new statistical method, H12, to detect both hard and soft selective sweeps in genomic data, revealing that recent adaptation in North American Drosophila melanogaster predominantly involves soft sweeps.

Contribution

The paper develops a novel haplotype homozygosity-based test, H12, capable of detecting soft sweeps, and applies it to identify recent adaptive events in Drosophila melanogaster.

Findings

Multiple genomic regions show signatures of soft sweeps.

Soft sweeps are more common than hard sweeps in recent Drosophila adaptation.

H12 and H2/H1 statistics effectively distinguish soft from hard sweeps.

Abstract

Rapid adaptation has been observed in numerous organisms in response to selective pressures, such as the application of pesticides and the presence of pathogens. When rapid adaptation is driven by rare alleles from the standing genetic variation or by a high population rate of de novo adaptive mutation, positive selection should commonly generate soft rather that hard selective sweeps. In a soft sweep, multiple adaptive haplotypes sweep through the population simultaneously, in contrast to hard sweeps in which only a single adaptive haplotype rises to high frequency. Current statistical methods were not designed to detect soft sweeps, and are therefore likely to miss these possibly numerous adaptive events. Here, we develop a statistical test (H12) based on haplotype homozygosity that is capable of detecting both hard and soft sweeps with similar power. We use H12 to identify multiple genomic regions that have undergone recent and strong adaptation in a population sample of fully sequenced Drosophila melanogaster strains from the Drosophila Genetic Reference Panel (DGRP). Visual inspection of the top 50 peaks revealed that multiple haplotypes are at high frequency, consistent with signatures of soft sweep. We developed a second statistic (H2/H1) that is sensitive to signatures common to soft sweeps but not hard sweeps, in order to determine whether sweeps detected by H12 can be more easily generated by hard versus soft sweeps. Surprisingly, we find that the H12 and H2/H1 values for all top 50 peaks are more easily generated by soft sweeps than hard sweeps under several evolutionary scenarios.