Spatial structure alters the allele frequency spectrum produced by hitchhiking

The reduction of genetic diversity due to genetic hitchhiking is widely used to find past selective sweeps from sequencing data, but very little is known about how spatial structure affects hitchhiking. We use mathematical modeling and simulations to find the unfolded allele-frequency-spectrum (AFS) left by hitchhiking in the genomic region of a sweep in a population occupying a one-dimensional range. For such populations, sweeps spread as Fisher waves, rather than logistically. We find that this leaves a characteristic three-part AFS at loci very close to the swept locus. Very low frequencies are dominated by recent mutations that occurred after the sweep and are unaffected by hitchhiking. At moderately low frequencies, there is a transition zone primarily composed of alleles that briefly “surfed” on the wave of the sweep before falling out of the wave front, leaving a spectrum close to that expected in well-mixed populations. However, for moderate-to-high frequencies, there is a distinctive scaling regime of the AFS produced by alleles that drifted to fixation in the wavefront and then were carried throughout the population. For loci slightly farther away from the swept locus on the genome, recombination limits the lifetime of alleles in the wavefront and introduces a fourth scaling regime. We find that these signatures of space can be strong even in apparently well-mixed populations with negligible spatial genetic differentiation, suggesting that space frequently distorts the signatures of hitchhiking in nature.