Deleterious variation shapes the genomic landscape of introgression

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.Author summary: Individuals from distinct populations sometimes will produce fertile offspring and will exchange genetic material in a process called hybridization. Genomes of hybrid individuals often show non-random patterns of hybrid ancestry across the genome, where some regions have a high frequency of ancestry from the second population and other regions have less. Typically, this pattern has been attributed to adaptive introgression, where beneficial genetic variants are passed from one population to the other, or to genomic incompatibilities between these distinct species. However, other mechanisms could lead to these heterogeneous patterns of ancestry in hybrids. Here we use simulations to investigate whether deleterious mutations affect the patterns of introgressed ancestry across genomes. We show that when ancestry from a larger population is added to a smaller population, the ancestry from the larger population dramatically increases in frequency because it carries fewer deleterious mutations. This occurs even in the absence of beneficial mutations in either population. Additionally, we show that differences in sex chromosome evolution relative to autosomes, or differences in mating system, can affect patterns of introgression in similar ways. Our study argues that deleterious mutations should be included in population genetic models used to identify unusual regions of the genome that appear to be under selection in hybrids.