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

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

Sex Differences in Recombination in Sticklebacks.

Recombination often differs markedly between males and females. Here we present the first analysis of sex-specific recombination in Gasterosteus sticklebacks. Using whole-genome sequencing of 15 crosses between G. aculeatus and G. nipponicus, we localized 698 crossovers with a median resolution of 2.3 kb. We also used a bioinformatic approach to infer historical sex-averaged recombination patterns for both species. Recombination is greater in females than males on all chromosomes, and overall map length is 1.64 times longer in females. The locations of crossovers differ strikingly between sexes. Crossovers cluster toward chromosome ends in males, but are distributed more evenly across chromosomes in females. Suppression of recombination near the centromeres in males causes crossovers to cluster at the ends of long arms in acrocentric chromosomes, and greatly reduces crossing over on short arms. The effect of centromeres on recombination is much weaker in females. Genomic differentiation between G. aculeatus and G. nipponicus is strongly correlated with recombination rate, and patterns of differentiation along chromosomes are strongly influenced by male-specific telomere and centromere effects. We found no evidence for fine-scale correlations between recombination and local gene content in either sex. We discuss hypotheses for the origin of sexual dimorphism in recombination and its consequences for sexually antagonistic selection and sex chromosome evolution

Searching for signatures of sexually antagonistic selection on stickleback sex chromosomes.

Intralocus sexually antagonistic selection occurs when an allele is beneficial to one sex but detrimental to the other. This form of selection is thought to be key to the evolution of sex chromosomes but is hard to detect. Here we perform an analysis of phased young sex chromosomes to look for signals of sexually antagonistic selection in the Japan Sea stickleback (Gasterosteus nipponicus). Phasing allows us to date the suppression of recombination on the sex chromosome and provides unprecedented resolution to identify sexually antagonistic selection in the recombining region of the chromosome. We identify four windows with elevated divergence between the X and Y in the recombining region, all in or very near genes associated with phenotypes potentially under sexually antagonistic selection in humans. We are unable, however, to rule out the alternative hypothesis that the peaks of divergence result from demographic effects. Thus, although sexually antagonistic selection is a key hypothesis for the formation of supergenes on sex chromosomes, it remains challenging to detect. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'

Patterns of Population Structure and Introgression Among Recently Differentiated \u3ci\u3eDrosophila melanogaster\u3c/i\u3e Populations

Despite a century of genetic analysis, the evolutionary processes that have generated the patterns of exceptional genetic and phenotypic variation in the model organism Drosophila melanogaster remains poorly understood. In particular, how genetic variation is partitioned within its putative ancestral range in Southern Africa remains unresolved. Here, we study patterns of population genetic structure, admixture, and the spatial structuring of candidate incompatibility alleles across a global sample, including 223 new accessions, predominantly from remote regions in Southern Africa. We identify nine major ancestries, six that primarily occur in Africa and one that has not been previously described. We find evidence for both contemporary and historical admixture between ancestries, with admixture rates varying both within and between continents. For example, while previous work has highlighted an admixture zone between broadly defined African and European ancestries in the Caribbean and southeastern USA, we identify West African ancestry as the most likely African contributor. Moreover, loci showing the strongest signal of introgression between West Africa and the Caribbean/southeastern USA include several genes relating to neurological development and male courtship behavior, in line with previous work showing shared mating behaviors between these regions. Finally, while we hypothesized that potential incompatibility loci may contribute to population genetic structure across the range of D. melanogaster; these loci are, on average, not highly differentiated between ancestries. This work contributes to our understanding of the evolutionary history of a key model system, and provides insight into the partitioning of diversity across its range

A graphical illustration of Eq (9), demonstrating the size at which the introgressing haplotype is most strongly selected against versus the fraction of the haplotype that carries ancestral/replacement alleles.

The above shape is consistent for all values of parameters, and values are all positive when between and within population epistasis are opposite signs or are both positive. The code underlying this figure can be located in S1 File. (EPS)</p

Results for a haploid model.

(A) When divergence (b) is low, even fairly small introgressing haplotypes carry sufficient positive interactions between introgressed derived alleles to cancel out potential deleterious effects. As divergence increases, however, the fitness of smaller haplotypes rapidly declines, and it takes increasingly larger haplotypes to cancel out potential DMIs. If each allele has only direct negative selection on it in the receiving population (solid black line), a simple linear relationship in fitness is expected. Note that we assume direct selection on each allele is on average negative, and so the positive selection is entirely driven by epistasis. (B) When the introgressing haplotype is only carrying novel alleles (f = 0), increasing the number of alleles introgressing introduces increasing amounts of positive epistasis. However, as it replaces more and more of existing substitutions in the receiving population, it becomes more and more strongly selected against. In both panels, it is assumed all alleles are carrying either new or ancestral variants, with no replacement alleles (xreplacement = 0). Solid lines show exact numeric solutions, while dashed lines show approximations from Eq (5). The code underlying this figure can be located in S1 File.</p

Raw PBS values, including negative ones plotted against <i>f</i>_D.

While both PBS values are negatively correlated with introgression, note that the vast majority of PBSWest values are close to 0, and the negative trend is driven in part by more positive than negative PBS values. On the other hand, a more clear negative relationship between PBSOOA2 and fD is observed. The code and data underlying this figure can be located in S1 File. (EPS)</p

Fig 4 -

(A) Previous work has identified an introgression event between Western African D. melanogaster (West) into North American populations (OOA2). South African populations (South1) are ancestral to both and used as an outgroup. Using previously published data, we calculated branch scores (normalized Population Branch Statistics), for 25,874 windows across the genome with some evidence for introgression. fD statistics were calculated using the population relationship shown in A, with OOA1 as a sister population with OOA2. (B) The genome-wide density of relative branch scores is clustered at values indicating high differentiation between OOA2 and both of the other populations (red values—high density, blue—low). However, the higher introgression windows (fD > 0.5) are depleted for long OOA2 branches and show many more windows with longer West and South1 branches. (C) Density plot of recombination rate versus fD, each bin is colored by the number of windows within the bin. A negative relationship between local recombination rate and introgression exists for all windows with fD >0 and (D) a similar negative relationship exists for OOA2 branch score and introgression, indicating diverged windows are more resilient to introgression. No significant relationship between West branch length and fD was identified. Slopes and p-values are from individual linear models for each plot. The code and data underlying this figure can be located in S1 File.</p

Outline of model assumptions.

(A) Two populations (A and B) evolve independently, fixing substitutions in their genome, represented by filled bars, until introgression at some point moves alleles from A into B. (B) Three types of alleles may introgress as a result: new alleles which are derived in A and ancestral in B (blue fill), ancestral alleles which are ancestral in A and derived in B (dashed outline) and replacement alleles in which both A and B have fixed alternate variants (dashed outline, blue fill). Each of these types of alleles will on average have different fitness effects, and either introduce new epistatic interactions (solid arrows), or remove existing ones (dashed arrows) (C) An introgressing haplotype of length x carrying all 3 types of alleles will both introduce novel epistatic interactions (solid arrows) and remove existing ones (dashed) in individuals carrying the haplotype compared to others in the population.</p

Replacement alleles show similar effects to ancestral.

Examining how the selection coefficient on an introgressing haplotype changes as the fraction of substitutions it carries varies between new, ancestral, and replacement alleles, as in Fig 3 but using approximation in Eq (5). The code underlying this figure can be located in S1 File. (TIF)</p