Relaxed selection during a recent human expansion

Abstract

30Humans have colonized the planet through a series of range expansions, which deeply impacted 31 genetic diversity in newly settled areas and potentially increased the frequency of deleterious mutations 32 on expanding wave fronts. To test this prediction, we studied the genomic diversity of French Canadians 33 who colonized Quebec in the 17 th century. We used historical information and records from ~4000 34 ascending genealogies to select individuals whose ancestors lived mostly on the colonizing wave front 35 and individuals whose ancestors remained in the core of the settlement. Comparison of exomic diversity 36 reveals that i) both new and low frequency variants are significantly more deleterious in front than in 37 core individuals, ii) equally deleterious mutations are at higher frequencies in front individuals, and iii) 38 front individuals are two times more likely to be homozygous for rare very deleterious mutations 39 present in Europeans. These differences have emerged in the past 6-9 generations and cannot be 40 explained by differential inbreeding, but are consistent with relaxed selection on the wave front. 41Modeling the evolution of rare variants allowed us to estimate their associated selection coefficients as 42 well as front and core effective sizes. Even though range expansions had a limited impact on the overall 43 fitness of French Canadians, they could explain the higher prevalence of recessive genetic diseases in 44 recently settled regions. Since we show that modern human populations are experiencing differential 45 strength of purifying selection, similar processes might have happened throughout human history, 46 contributing to a higher mutation load in populations that have undergone spatial expansions. 47 48.

Selfing ability and drift load evolve with range expansion

“…Recurrent founder events during colonization should reduce effective population size (Wade & McCauley 1988;Peter & Slatkin 2013), particularly if successful founders are drawn from locations near the wave front (Hallatschek & Nelson 2008). In these cases, an accumulation of deleterious mutations known as the expansion load (or drift load) may occur (Peischl et al 2013;Henn et al 2016;Peischl et al 2018). Crosses between populations with high expansion load should yield heterosis or hybrid vigor, particularly for those with the smallest effective sizes (Whitlock et al 2000;Oakley et al 2015;Spigler et al 2017;Willi et al 2018).…”

The fitness consequences of genetic variation in wild populations of mice

“…We have a growing sense of the strength of selection acting on phenotypes 9,39-42 , and there is now extensive data providing statistical signatures of historical selection on the genome [43][44][45][46] . However, uncertainty remains concerning the magnitude and causes of genetic changes that occur as populations evolve under new ecological conditions [47][48][49][50] . Our experimental design mimics the replicated and reciprocal colonization of divergent habitats by populations carrying sequence variants that cause functional changes in a locally adapted phenotype.…”

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

“…Theory predicts that gene surfing can also apply to mildly deleterious mutations (Travis et al, 2007), thus creating an 'expansion load' if these mutations become fixed (Peischl et al, 2013). Recent analyses of genetic structure in human populations (Peischl et al, 2018) and laboratory experiments on bacterial populations (Bosshard et al, 2017) provided consistent evidence in support of this expansion load hypothesis. 'Pushed' and 'pulled' expansion All of the above predictions arise from the interplay of demographic and evolutionary processes operating at lowdensity populations at the expanding front.…”