The Impact of Genetic Surfing on Neutral Genomic Diversity

Abstract

Range expansions have been common in the history of most species. Serial founder effects and subsequent population growth at expansion fronts typically lead to loss of genomic diversity along the expansion axis. A frequent consequence is the phenomenon of “gene surfing”, where variants located near the expanding front can reach high frequencies or even fix in newly colonized territories. Although gene surfing events have been characterized thoroughly for a specific locus, their effects on linked genomic regions and on the overall patterns of genomic diversity have been little investigated. In this study, we simulated the evolution of whole genomes during several types of 1D and 2D range expansions differing by the extent of migration, founder events and recombination rates. We focused on the characterization of local dips of diversity, or “troughs”, taken as a proxy for surfing events. We find that, for a given recombination rate, once we consider the amount of diversity lost since the beginning of the expansion, it is possible to predict the initial evolution of trough density and their average width irrespectively of the expansion condition. Furthermore, when recombination rates vary across the genome, we find that troughs are over-represented in regions of low recombination. Therefore, range expansions can leave local and global genomic signatures often interpreted as evidence of past selective events. Given the generality of our results, they could be used as a null model for species having gone through recent expansions, and thus be helpful to correctly interpret many evolutionary biology studies.

The landscape of nucleotide diversity in Drosophila melanogaster is shaped by mutation rate variation

“…From a practical standpoint, it means that drift should not be neglected as an explanation for the distribution of π, especially at narrow window sizes (≤ 10 kb). This is relevant because it is also at narrow window sizes that the effect of selection on diversity levels along the genome can be more easily confounded by the effect of drift, with extreme examples happening during population range expansions and especially in regions of low recombination (Schlichta et al, 2022).…”

The landscape of nucleotide diversity inDrosophila melanogasteris shaped by mutation rate variation

“…From a practical standpoint, it means that drift should not be neglected as an explanation for the distribution of π, especially at narrow window sizes (<=10 kb). This is relevant because it is also at narrow window sizes that the effect of selection on diversity levels along the genome can be more easily confounded by the effect of drift, with extreme examples happening during population range expansions and especially on regions of low recombination (Schlichta et al, 2022).…”

The genetic consequences of range expansion and its influence on diploidization in polyploids

“…As a result, populations on the edge of an expansion should have reduced fitness compared to populations in the core. Although the primary consequence of this process is reduced fitness, range expansions can alter the landscape of neutral genetic diversity across the genome (Schlichta et al 2022) and can promote the hybridization of species coming into secondary contact (MacPherson et al 2022).…”

“…As a result, populations on the edge of an expansion should have reduced fitness compared to populations in the core. Although the primary consequence of this process is reduced fitness, range expansions can alter the landscape of neutral genetic diversity across the genome (Schlichta et al 2022) and can promote the hybridization of species coming into secondary contact (MacPherson et al 2022). However, research on the consequences of range expansions have not been conducted in polyploids, and it is not currently known whether a geographically expanding polyploid population would experience stronger or milder consequences from a range expansion than an analogously expanding diploid population.…”