The fitness of an introgressing haplotype changes over the course of divergence and depends on its size and genomic location

Abstract

The genomic era has made clear that introgression, or the movement of genetic material between species, is a common feature of evolution. Examples of both adaptive and deleterious introgression exist in a variety of systems. What is unclear is how the fitness of an introgressing haplotype changes as species diverge or as the size of the introgressing haplotype changes. In a simple model, we show that introgression may more easily occur into parts of the genome which have not diverged heavily from a common ancestor. The key insight is that alleles from a shared genetic background are likely to have positive epistatic interactions, increasing the fitness of a larger introgressing block. In regions of the genome where few existing substitutions are disrupted, this positive epistasis can be larger than incompatibilities with the recipient genome. Further, we show that early in the process of divergence, introgression of large haplotypes can be favored more than introgression of individual alleles. This model is consistent with observations of a positive relationship between recombination rate and introgression frequency across the genome; however, it generates several novel predictions. First, the model suggests that the relationship between recombination rate and introgression may not exist, or may be negative, in recently diverged species pairs. Furthermore, the model suggests that introgression that replaces existing derived variation will be more deleterious than introgression at sites carrying ancestral variants. These predictions are tested in an example of introgression in Drosophila melanogaster, with some support for both. Finally, the model provides a potential alternative explanation to asymmetry in the direction of introgression, with expectations of higher introgression from rapidly diverged populations into slowly evolving ones.

Falling shoulders ahead: adaptive alien genes are maintained amid vanishing introgression footprint in sea squirts

“…We expect recombination in introgression tracts to uncouple this negative selection during the selective sweep, making the hitchhiking footprint narrower than in a standard selective sweep model in which the shoulders are neutral. This expectation is in line with the Dagilis & Matute (2023) model that suggests that short haplotypes are more likely to be introgressed than long haplotypes in divergent species where reproductive incompatibilities have evolved. Once the beneficial allele has fixed or stabilised in frequency, we can thus expect recombination to continue to uncouple negative selection on shorter linked tracts and purge the alien ancestry in the shoulder of an adaptive introgression sweep, and this should be all the stronger as the divergence between species is greater.…”

“…The first explanation is that introgression tracts that hitchhiked with the adaptive alien allele carry deleterious mutations in the native genetic background. Given the strong divergence between the two Ciona species, we expect most of the alien genome to be incompatible in the native genetic background and to be selected against when introgressed (Schneeman et al, 2020; Schiffman & Ralph, 2018, Dagilis & Matute, 2023). In addition, beneficial alleles must have high selective coefficients to overcome the combined effects of negative linked selection against their flanking neighbours in recipient populations (Edelman & Mallet, 2021).…”

“…The allele frequency was lowest at SNP 10 (0.02 ; 738,970 In contrast to the results for SNP 15, among the nine SNPs located in the shoulders of the introgression island, six (SNP 12,13,16,18,20 and 21) showed significant changes in C. robusta allele frequencies (Fisher's exact test in Table S5B). In addition, five of them (13,16,18,20,21) showed a significantly lower alien allele frequency in 2021 as compared with 2012 (Wicoxon-signed rank test; Table S5B) (Fig. 4).…”

Recent secondary contact, genome-wide admixture, and limited introgression of neo-sex chromosomes between two Pacific island bird species

“…Nevertheless, phenotypic hybrids and admixed individuals continue to be observed decades after colonization. It is therefore possible that introgression of maternally coinherited sequences from Mcard into Mtris genomic backgrounds occurs via asymmetric mate choice, is globally adaptive, or is driven by selfish W or neo-W [74,75]. Future work is necessary to distinguish these alternatives.…”

The recombination landscape of introgression in yeast

“…This positive correlation between introgressed ancestry and recombination is emerging as a nearly ubiquitous pattern (though see (Dagilis & Matute, 2023; Duranton & Pool, 2022; Pool, 2015)), however, it is unclear how these observations relate to the known effect of sequence divergence on DSB resolution. Introgression, particularly between highly diverged species, can have low sequence homology with the genomic region it is replacing.…”