Hybrid fitness effects modify fixation probabilities of introgressed alleles

Pfennig, Aaron; Lachance, Joseph

doi:10.1093/g3journal/jkac113

Cited by 4 publications

(8 citation statements)

References 59 publications

(84 reference statements)

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“…Early in divergence, this may dampen the benefits of keeping large blocks intact, as individuals may carry many unlinked co-adapted introgressing alleles that weaken selection against any individual introgressing allele. More broadly, this means that multiple haplotypes of varying sizes are likely to be introgressing, making predictions far less straightforward [ 21 , 22 , 31 ].…”

Section: Discussionmentioning

confidence: 99%

“…On the one hand, alleles acting as barriers to gene flow (due to lower fitness in the recipient genome) may impede introgression of nearby neutral alleles [ 3 ] or even positively selected alleles [ 23 ]. If heterozygotes experience higher fitness due to overdominance of alleles, the introgression probability of neutral alleles may be increased [ 22 ], even when deleterious epistasis between an introgressed haplotype block and the recipient genome is frequent. If selection on introgressed alleles is positive, but distributed broadly across introgressing regions, adaptive blocks may be maintained at intermediate sizes due to linkage between many individually selected alleles [ 32 ].…”

Section: Introductionmentioning

confidence: 99%

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

Dagilis

Matute

2023

PLoS Biol

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Dagilis

Matute

2023

PLoS Biol

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“…Early in divergence, this may dampen the benefits of keeping large blocks intact. More broadly, this means that multiple haplotypes of varying sizes are likely to be introgressing, making predictions far less straightforward (Veller et al 2021; Duranton and Pool 2022; Pfennig and Lachance 2022).…”

Section: Discussionmentioning

confidence: 99%

“…Empirical evidence of positive selection of introgressed alleles is extensive (see Edelman and Mallet (2021) for a review). Positive effects of introgression have demonstrated how heterotic effects resulting from overdominance can increase the probability of neutral markers introgressing (Pfennig and Lachance 2022) even when deleterious epistasis with the host genome is frequent. However, introgressing haplotypes are likely to carry epistatic interactions not only with the receiving genome, but also among the introgressing alleles as well.…”

Section: Introductionmentioning

confidence: 99%

“…Generally, these models find that there is a “grey zone” of speciation - when hybrid fitness is reduced, yet remains high enough that hybrids between the two species survive and mate sufficiently to enable gene flow between the species (Roux et al 2016). There are many fewer models of introgression, and those that exist generally assume that introgression is primarily deleterious (Harris and Nielsen 2016; Martin and Jiggins 2017; Petr et al 2019; Veller et al 2021; Pfennig and Lachance 2022), however we know that sometimes introgression is adaptive (Huerta-Sánchez et al 2014; Norris et al 2015; Edelman and Mallet 2021), and so what types of loci and what fraction of the genome in general can introgress remains unknown, but it is likely that introgressed regions are rarely neutral.…”

Section: Introductionmentioning

confidence: 99%

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The fitness of an introgressing haplotype

Dagilis

Matute

2022

Preprint

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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 early in the process of divergence, introgression of large haplotypes can be favored more than introgression of individual alleles. 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. The buildup of incompatibilities between diverging species in the form of deleterious epistasis eventually favors the introgression of small haplotypes as the number of diverged alleles increases, and eventually even single alleles with positive direct effects can be selected against. 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 always be more deleterious than introgression at sites carrying ancestral variants. These predictions are tested in an example of introgression in D. melanogaster, with some support for both.

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The evolutionary fate of Neanderthal DNA in 30,780 admixed genomes with recent African-like ancestry

Pfennig,

Lachance

2024

Preprint

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Following introgression, Neanderthal DNA was initially purged from non-African genomes, but the evolutionary fate of remaining introgressed DNA has not been explored yet. To fill this gap, we analyzed 30,780 admixed genomes with African-like ancestry from the All of Us research program, in which Neanderthal alleles encountered novel genetic backgrounds during the last 15 generations. Observed amounts of Neanderthal DNA approximately match expectations based on ancestry proportions, suggesting neutral evolution. Nevertheless, we identified genomic regions that have significantly less or more Neanderthal ancestry than expected and are associated with spermatogenesis, innate immunity, and other biological processes. We also identified three novel introgression desert-like regions in recently admixed genomes, whose genetic features are compatible with hybrid incompatibilities and intrinsic negative selection. Overall, we find that much of the remaining Neanderthal DNA in human genomes is not under strong selection, and complex evolutionary dynamics have shaped introgression landscapes in our species.

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Hybrid fitness effects modify fixation probabilities of introgressed alleles

Cited by 4 publications

References 59 publications

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

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

The fitness of an introgressing haplotype

The evolutionary fate of Neanderthal DNA in 30,780 admixed genomes with recent African-like ancestry

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