Deleterious variation shapes the genomic landscape of introgression

Abstract

While it is appreciated that population size changes can impact patterns of deleterious variation in natural populations, less attention has been paid to how gene flow affects and is affected by the dynamics of deleterious variation. Here we use population genetic simulations to examine how gene flow impacts deleterious variation under a variety of demographic scenarios, mating systems, dominance coefficients, and recombination rates. Our results show that admixture between populations can temporarily reduce the genetic load of smaller populations and cause increases in the frequency of introgressed ancestry, especially if deleterious mutations are recessive. Additionally, when fitness effects of new mutations are recessive, between-population differences in the sites at which deleterious variants exist creates heterosis in hybrid individuals. Together, these factors lead to an increase in introgressed ancestry, particularly when recombination rates are low. Under certain scenarios, introgressed ancestry can increase from an initial frequency of 5% to 30–75% and fix at many loci, even in the absence of beneficial mutations. Further, deleterious variation and admixture can generate correlations between the frequency of introgressed ancestry and recombination rate or exon density, even in the absence of other types of selection. The direction of these correlations is determined by the specific demography and whether mutations are additive or recessive. Therefore, it is essential that null models of admixture include both demography and deleterious variation before invoking other mechanisms to explain unusual patterns of genetic variation.

The role of recombination on genome‐wide patterns of local ancestry exemplified by supplemented brook charr populations

“…This may reflect a positive effect (i.e., associative over‐dominance) of the presence of domestic ancestry in these regions. This interpretation is congruent with the hypothesis of temporarily reduced genetic load, caused by the masking of deleterious mutations, and resulting in an increase of introgressed ancestry as observed in a simulation study (Kim et al, ). This is also consistent with the expected higher accumulation of deleterious mutations in small lacustrine brook charr populations as observed by Ferchaud et al () as well as with the higher allelic richness observed in the domestic strain compared to these small lacustrine populations (Martin et al, ).…”

“…Second, given the generally small effective population size of these brook charr lacustrine populations (Gossieux, Bernatchez, Sirois, & Garant, ), random drift may also be responsible for variable ancestry locally along the genome (Martin & Jiggins, ) and is not expected to produce consistent patterns across lakes. Third, the most likely evolutionary mechanism that could explain the general negative correlation would be a dominant effect of associative overdominance (Kim et al, ). Indeed, favoured domestic ancestry within regions of low recombination rate is likely to reflect the action of associative‐overdominance, especially if the recipient population tends to accumulate recessive deleterious alleles preferentially in low‐recombining regions (Charlesworth & Willis, ).…”

“…Indeed, favoured domestic ancestry within regions of low recombination rate is likely to reflect the action of associative‐overdominance, especially if the recipient population tends to accumulate recessive deleterious alleles preferentially in low‐recombining regions (Charlesworth & Willis, ). Consequently, long introgressed foreign haplotypes of domestic origin would be favoured by masking the effect of linked recessive deleterious mutations present in the small local populations (i.e., local heterosis effect; Charlesworth & Willis, ; Kim et al, ). Kim et al () suggested that the presence of slightly deleterious recessive mutations might modulate the genome‐wide introgression rate in hybrid populations.…”

“…However, the occurrence of multiple hybrid incompatibilities seems unlikely here as the domestic stain is not highly divergent from the wild populations. Finally, (c) in the situation of selection against domestic haplotypes due to unconditionally deleterious introgression (or hybridization load), foreign loci of small individual effect are expected to be removed more quickly within low‐recombining regions because selection is more effective in removing linked deleterious mutations (Kim et al, ; Martin & Jiggins, ; Schumer et al, ). We observed such a pattern for two LGs (7 and 41) displaying a deficit of domestic introgression in the presence of potentially deleterious mutations.…”

Ancestral and neo‐sex chromosomes contribute to population divergence in a dioecious plant

“…This disproportionate accumulation of deleterious variants on the Y may explain low rates of gene flow on the Y if, for example, selection is more effective in one population than another. Recent work simulating gene flow patterns between humans and Neanderthals, as well as between species of Arabidopsis, found that the gene flow landscape could be best explained by the differential accumulation of deleterious variation between genomic regions (Kim et al 2018). Similarly, lowered efficacy of selection on the Y due to linked selection could be an important driver of reduced gene flow on the Y chromosomes of R. hastatulus.…”