Strong neutral sweeps occurring during a population contraction

Abstract

A strong reduction in diversity around a specific locus is often interpreted as a recent rapid fixation of a positively selected allele, a phenomenon called a selective sweep. Rapid fixation of neutral variants can however lead to similar reduction in local diversity, especially when the population experiences changes in population size, e.g., bottlenecks or range expansions. The fact that demographic processes can lead to signals of nucleotide diversity very similar to signals of selective sweeps is at the core of an ongoing discussion about the roles of demography and natural selection in shaping patterns of neutral variation. Here we quantitatively investigate the shape of such neutral valleys of diversity under a simple model of a single population size change, and we compare it to signals of a selective sweep. We analytically describe the expected shape of such “neutral sweeps” and show that selective sweep valleys of diversity are, for the same fixation time, wider than neutral valleys. On the other hand, it is always possible to parametrize our model to find a neutral valley that has the same width as a given selected valley. Our findings provide further insight in how simple demographic models can create valleys of genetic diversity similar to those attributed to positive selection.

The Impact of Genetic Surfing on Neutral Genomic Diversity

“…Indeed, many candidate loci for positive selection have been identified in regions of low recombination in humans ( O’Reilly et al 2008 ). The fact that troughs caused by neutral sweeps also tend to span regions of low recombination is important since it shows that a purely neutral process can reproduce a signal previously attributed to selection at the whole-genome level and not only at the single-locus level ( Koropoulis et al 2020 ; Moinet et al 2022 ).…”

“…It would be tempting to apply our findings to real world data, by examining the distribution of troughs over the genome of some species having gone through some recent range expansion, but precise knowledge of the effect of BGS and population recovery on neutral sweeps may be required before such an attempt. In any case, since selected sweeps and neutral sweeps could lead to very similar dips of diversity at individual loci ( Moinet et al 2022 ), it seems that the distinction between selection and demography would be better achieved by examining overall genomic patterns rather than looking at individual windows ( Schrider and Kern 2018 ). In this respect, an interesting goal would be to infer the likelihood of a given distribution of trough density and size predicted from a given distribution of fitness effect previously inferred from patterns of genomic diversity ( Kim et al 2017 ; Tataru and Bataillon 2020 ) and compare it to that expected under a range expansion scenario.…”

“…Range expansions also influence patterns of introgression and hybridization, namely enabling asymmetric introgression between species ( Currat et al 2008 ), an important factor to account for in speciation genomics. Finally, recent studies have shown that both positive selection and population contractions can lead to similar “dips of diversity” along the genome (hereafter called “troughs”) and that these selective and neutral sweeps can easily be confounded when analyzing single locus empirical data ( Moinet et al 2022 ).…”

Natural selection and neutral mutations through the lens of viruses

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The Neutral Theory and the Modern Synthesis, a modified version of Darwin's theory, have been arguing for decades about the influence of natural selection on molecular evolution [1][2][3][4][5][6][7][8][9][10] . Here we elucidate through the lens of viruses that a frequently used method [11][12][13][14][15][16][17] employing the ratio of nonsynonymous versus synonymous substitution rates has dramatically underestimated the influence of natural selection on molecular evolution.

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“…By contrast, the Neutral Theory, which was established after the Modern Synthesis, holds that molecular evolution mainly depends on random genetic drift of neutral mutations [7][8][9][10] . Biologists have been debating these two contradictory views for decades [1][2][3][4][5][6] .…”