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.

Patterns of Population Structure and Introgression Among Recently Differentiated Drosophila melanogaster 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.

What inversion lengths can tell us about their evolution.

Genome structural differences, such as inversions, are extremely common between species and within populations. Theoretical models of how and why such inversions evolve have affirmed that they are able to evolve under both adaptive and nonadaptive scenarios (reviewed in Kirkpatrick, 2010). What has remained difficult, however, is distinguishing these scenarios from each other. In this issue of Molecular Ecology, Connallon and Olito (2022) present a model that examines how adaptive and nonadaptive scenarios lead to different distributions of inversion sizes. The authors present several important predictions including an expectation that larger inversions should evolve under local adaptation scenarios and much smaller inversions should evolve when they are either underdominant or directly beneficial. Finally, the authors ask how the presence of deleterious mutations within populations affects the probability of fixing inversions of different types. The study is therefore an important step in synthesizing decades of inversion theory.

The evolution of hybrid fitness during speciation.

The evolution of postzygotic reproductive isolation is an important component of speciation. But before isolation is complete there is sometimes a phase of heterosis in which hybrid fitness exceeds that of the two parental species. The genetics and evolution of heterosis and postzygotic isolation have typically been studied in isolation, precluding the development of a unified theory of speciation. Here, we develop a model that incorporates both positive and negative gene interactions, and accounts for the evolution of both heterosis and postzygotic isolation. We parameterize the model with recent data on the fitness effects of 10,000 mutations in yeast, singly and in pairwise epistatic combinations. The model makes novel predictions about the types of interactions that contribute to declining hybrid fitness. We reproduce patterns familiar from earlier models of speciation (e.g. Haldane's Rule and Darwin's Corollary) and identify new mechanisms that may underlie these patterns. Our approach provides a general framework for integrating experimental data from gene interaction networks into speciation theory and makes new predictions about the genetic mechanisms of speciation.

Admixture in the fungal pathogen Blastomyces.

Blastomyces is an emerging primary fungal pathogen that affects patients worldwide. The evolutionary processes that have resulted in the current diversity in the genus remain largely unexplored. We used whole genome sequences from 99 Blastomyces isolates, including two sequenced in this study using long-read technologies, to infer the phylogenetic relationships between Blastomyces species. We find that five different methods infer five different phylogenetic trees. Additionally, we find gene tree discordance along the genome with differences in the relative phylogenetic placement of several species of Blastomyces, which we hypothesize is caused by introgression. Our results suggest the urgent need to systematically collect Blastomyces samples around the world and study the evolutionary processes that govern intra- and interspecific variation in these medically important fungi.

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'.

A need for standardized reporting of introgression: Insights from studies across eukaryotes.

With the rise of affordable next-generation sequencing technology, introgression-or the exchange of genetic materials between taxa-has become widely perceived to be a ubiquitous phenomenon in nature. Although this claim is supported by several keystone studies, no thorough assessment of the frequency of introgression across eukaryotes in nature has been performed to date. In this manuscript, we aim to address this knowledge gap by examining patterns of introgression across eukaryotes. We collated a single statistic, Patterson's D, which can be used as a test for introgression across 123 studies to further assess how taxonomic group, divergence time, and sequencing technology influence reports of introgression. Overall, introgression has mostly been measured in plants and vertebrates, with less attention given to the rest of the Eukaryotes. We find that the most frequently used metrics to detect introgression are difficult to compare across studies and even more so across biological systems due to differences in study effort, reporting standards, and methodology. Nonetheless, our analyses reveal several intriguing patterns, including the observation that differences in sequencing technologies may bias values of Patterson's D and that introgression may differ throughout the course of the speciation process. Together, these results suggest the need for a unified approach to quantifying introgression in natural communities and highlight important areas of future research that can be better assessed once this unified approach is met.

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.

Systematic analysis of complex genetic interactions.

To systematically explore complex genetic interactions, we constructed ~200,000 yeast triple mutants and scored negative trigenic interactions. We selected double-mutant query genes across a broad spectrum of biological processes, spanning a range of quantitative features of the global digenic interaction network and tested for a genetic interaction with a third mutation. Trigenic interactions often occurred among functionally related genes, and essential genes were hubs on the trigenic network. Despite their functional enrichment, trigenic interactions tended to link genes in distant bioprocesses and displayed a weaker magnitude than digenic interactions. We estimate that the global trigenic interaction network is ~100 times as large as the global digenic network, highlighting the potential for complex genetic interactions to affect the biology of inheritance, including the genotype-to-phenotype relationship.

Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions.

Chromosomal inversions are frequently implicated in isolating species. Models have shown how inversions can evolve in the context of postmating isolation. Inversions are also frequently associated with mating preferences, a topic that has not been studied theoretically. Here, we show how inversions can spread by capturing a mating preference locus and one or more loci involved with epistatic incompatibilities. Inversions can be established under broad conditions ranging from near panmixis to nearly complete speciation. These results provide a hypothesis to explain the growing number of examples of inversions associated with premating isolating mechanisms.