Evolution of functional genomic diversity during a bottleneck

Abstract

Most species have been through population bottlenecks and range expansions, and the impact of these events on patterns of diversity has been well studied. In particular, it has been shown that initially rare neutral variants could readily fix on the front of range expansions or during bottlenecks, giving genomic signatures looking like selective sweeps. Here we expand on previous work by considering the dynamics of genomic diversity in (functional) regions harbouring deleterious variants during bottlenecks or during range expansions modelled as serial founder effects. We find that regions with very low levels of diversity (troughs) looking like selective sweeps can also readily form in these functional regions. Additionally, their properties depend on the dominance level of deleterious mutations. Trough density is higher and increases more rapidly in regions with co-dominant deleterious mutations than in regions with recessive mutations. Interestingly, we find that genetic diversity declines less rapidly in regions with partially recessive mutations than in regions with codominant ones or in regions with only neutral mutations. These features are generally enhanced in low recombination regions and for intermediate selection coefficients. If most deleterious mutations in a genome are partially recessive, it follows that functional low recombination regions should better preserve genetic diversity during range expansions than neutral regions of the genome. Significance statementMost research on the effects of selection on genetic diversity have been done in equilibrium populations, leaving a gap in our understanding of how selection acting on functional regions interacts with demographic changes. Our study reveals strikingly different impacts of purifying selection on genetic diversity depending on the dominance coefficient of deleterious mutations. While codominant variants create diversity dips resembling selective sweeps, recessive mutations can preserve genetic diversity during bottlenecks through the relatively understudied phenomenon of pseudo-overdominance. Our findings show how selective and demographic forces interact in more complex ways than previously thought and emphasize the importance of further exploring these dynamics to accurately interpret genetic variation in natural populations.