Spatial structure alters the site frequency spectrum produced by hitchhiking

Abstract

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 site frequency spectrum (SFS) 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 SFS 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 wavefront, 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 SFS 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 is much more effective at restoring diversity in one-dimensional populations than it is in well-mixed ones. We find that these signatures of space can be strong even in apparently well-mixed populations with negligible spatial genetic differentiation, suggesting that spatial structure may frequently distort the signatures of hitchhiking in natural populations.

Simulating the effects of long‐distance dispersal and landscape heterogeneity on the eco‐evolutionary outcomes of range expansion in an invasive riverine fish, Tench (Tinca tinca)

“…Finally, while our models focused on neural dynamics and patterns of genetic diversity derived from unlinked neutral loci, adaptive processes are known to influence neutral genetic diversity during range expansions. For example, neutral alleles located close to beneficially adaptive mutations can increase in frequency as adaptive alleles become fixed in the population (hitchhiking) (Gillespie, 2000; Min et al, 2022; Smith & Haigh, 1974). Alternatively, neutral variants linked to mutations with adverse fitness consequences might decrease in frequency as deleterious alleles are purged from the population (background selection) (Charlesworth et al, 1993).…”

Resource-explicit interactions in spatial population models

“…However, it may not be well-suited to populations that inhabit larger continuous landscapes. For such populations, it is often critical to model continuous space explicitly to capture key aspects of the evolutionary dynamics, such as the wave of advance of a strongly beneficial allele or the spread of an invasive species where it has been newly introduced 8,[13][14][15][16][17] .…”

Population genetics meets ecology: a guide to individual-based simulations in continuous landscapes

“…Geography can have strong effects on patterns of genetic variation (Wright, 1943;Malécot, 1969;Rousset, 2000;Charlesworth et al, 2003;Battey et al, 2020;Min et al, 2022) and on evolutionary processes (Felsenstein, 1976;Uecker et al, 2014;Savolainen et al, 2007). Genetic differentiation is shaped by the movement of individuals, and hence distance and geographical features, as well as the spatio-temporal history of the species (Hewitt, 2011;.…”