Genetic surfing in human populations: from genes to genomes

Abstract

Genetic surfing describes the spatial spread and increase in frequency of variants that are not lost by genetic drift and serial migrant sampling during a range expansion. Genetic surfing does not modify the total number of derived alleles in a population or in an individual genome, but it leads to a loss of heterozygosity along the expansion axis, implying that derived alleles are more often in homozygous state. Genetic surfing also affects selected variants on the wave front, making them behave almost like neutral variants during the expansion. In agreement with theoretical predictions, human genomic data reveals an increase in recessive mutation load with distance from Africa, an expansion load likely to have developed during the expansions of human populations out of Africa.

Direct evidence of an increasing mutational load in humans

“…Again, this is consistent with the demographic context, as this geographic region has been affected by at least three migration waves, associated with rapid demographic expansion(-s) [19]. Indeed, range expansions have been shown to enable new deleterious mutations to behave almost like neutral variants, hereby facilitating their increase in frequency [24]. This would suggest that (i) the deleterious mutations observed post-LGM are novel, i.e.…”

“…Altogether, the results presented here add temporal evidence to a debate that has mostly focused on space (as a proxy for time), to understand the relative strength of selection and demography in shaping the mutational load in human populations [34,35,36,24]. The crux of this debate actually hinges on the dominance of deleterious mutations, as theory predicts that load is greater under an additive model than under a recessive model [37], while both experimental [38] and empirical [20] evidence suggests that the most deleterious mutations are more likely to be recessive, but not always [39].…”

Loss of genetic diversity, recovery and allele surfing in a colonizing parasite, Geomydoecus aurei

“…The concept of "allele surfing" (Edmonds, Lillie, & Cavalli-Sforza, 2004; Klopfstein, Currat, & Excoffier, 2006) has emerged as having key explanatory power in modelled populations experiencing geographic range expansion, and the phenomenon has been observed both in cultured bacteria (e.g., Fusco, Gralka, Kayser, Anderson, & Hallatschek, 2016;Gralka et al, 2016;Hallatschek, Hersen, Ramanathan, & Nelson, 2007) and in eukaryotes in their natural environments (Becheler et al, 2016;François et al, 2010;Graciá et al, 2013;Peischl, Dupanloup, Bosshard, & Excoffier, 2016;Pierce et al, 2014;Streicher et al, 2016). Surfing allows rare alleles in a population to reach high frequency through repeated founder events and to become more widespread at the leading edge of population expansion (sometimes referred to as the wave front), where population density is especially low (Excoffier & Ray, 2008).…”

Mutation load dynamics during environmentally-driven range shifts

“…Furthermore, as 133 shifts proceed faster, population sizes are on average smaller at the front (Hallatschek 2008) 134 leading to more genetic drift and gene surfing. This decrease in N e leads to a higher probability 135 of fixation for deleterious alleles and a lower probability of fixation for beneficial alleles (Fig 136 2D, Peischl et al 2016), resulting in slower range shifts always exhibiting less fitness loss per 137 unit time (Fig 2A). The trade-off between efficacy of selection (more selection during slower 138 shifts) and the amount of influx of harmful mutations during a range shift (more mutations 139 during slower shifts) creates the non-monotonic behavior we find in both the analytic model and 140 simulations ( Fig 2B).…”