Heterogametic Research Articles

Making sense of recent models of the "sheltering" hypothesis for recombination arrest between sex chromosomes.

In their most extreme form, sex chromosomes exhibit a complete lack of genetic recombination along much of their length in the heterogametic sex. Some recent models explain the evolution of such suppressed recombination by the "sheltering" of deleterious mutations by chromosomal inversions that prevent recombination around a polymorphic locus controlling sex. This sheltering hypothesis is based on the following reasoning. An inversion that is associated with the male-determining allele (with male heterogamety) is present only in the heterozygous state. If such an inversion carries a lower-than-average number of deleterious mutations, it will accrue a selective advantage, and will be sheltered from homozygosity for any mutations that it carries due to the enforced heterozygosity for the inversion itself. It can therefore become fixed among all carriers of the male-determining allele. Recent population genetics models of this process are discussed. It is shown that, except under the unlikely scenario of a high degree of recessivity of most deleterious mutations, inversions of this type that lack any other fitness effects will have at best a modest selective advantage; they will usually accumulate on proto-Y chromosomes at a rate close to, or less than, the neutral expectation. While the existence of deleterious mutations does not necessarily prevent the spread of Y-linked inversions, it is unlikely to provide a significant selective advantage to them.

The Hypolimnas misippus Genome Supports a Common Origin of the W Chromosome in Lepidoptera.

Moths and butterflies (Lepidoptera) have a heterogametic sex chromosome system with females carrying ZW chromosomes and males ZZ. The lack of W chromosomes in early-diverging lepidopteran lineages has led to the suggestion of an ancestral Z0 system in this clade and a B chromosome origin of the W. This contrasts with the canonical model of W chromosome evolution in which the W would have originated from the same homologous autosomal pair as the Z chromosome. Despite the distinct models proposed, the rapid evolution of the W chromosome has hindered the elucidation of its origin. Here, we present high-quality, chromosome-level genome assemblies of 2 Hypolimnas species (Hypolimnas misippus and Hypolimnas bolina) and use the H. misippus assembly to explore the evolution of W chromosomes in butterflies and moths. We show that in H. misippus, the W chromosome has higher similarity to the Z chromosome than any other chromosome, which could suggest a possible origin from the same homologous autosome pair as the Z chromosome. However, using genome assemblies of closely related species (ditrysian lineages) containing assembled W chromosomes, we present contrasting evidence suggesting that the W chromosome might have evolved from a B chromosome instead. Crucially, by using a synteny analysis to infer homology, we show that W chromosomes are likely to share a common evolutionary origin in Lepidoptera. This study highlights the difficulty of studying the evolution of W chromosomes and contributes to better understanding its evolutionary origins.

Identification and mapping of sex-linked markers in giant abalone (Haliotis gigantea Gmelin)

Giant abalone (Haliotis gigantea Gmelin) is an economically important species within Haliotis genus, yet the genetic basis of sex in this species is still poorly understood. Therefore, we screened and mapped sex-linked SNPs and InDels, and subsequently developed a PCR-based method for genetic sex identification in giant abalone. Based on whole-genome sequencing reads, we obtained a total 6,159,941 high-quality SNPs and 2,623,263 high-quality InDels. Among them, 1,737 SNPs and 179 InDels were detected as sexually dimorphic, assuming a male heterogametic sex determination system. The majority of these variants, 99.1 % for SNPs and 99.4 % for InDels, were clustered on Chr.4 (0.02 Mb to 23.22 Mb). Furthermore, the estimation of genetic divergence between the sexes using FST showed that the genomic windows with the top 1 % FST values were concentrated on Chr.4 (0.5 Mb to 19.0 Mb) and Chr.5 (20.0 Mb to 35.0 Mb). Based on the sexually dimorphic variants on Chr.4, three PCR-based markers were successfully developed to determine the genetic sex of giant abalone. PCR validation using a tested panel of 67 females and 67 males from a cultivated population demonstrated compliance rates for these three markers ranging from 97.7 % to 99.3 %. These results suggest that the sex determination system is male heterogametic in giant abalone. Thus, this study provides valuable insights and tools for further research on the mechanisms of sex determination and differentiation, as well as for monitoring sex ratios in wild and cultivated populations in giant abalone.

Comparative Cytogenetics of the Malagasy Ground Geckos of the Paroedura bastardi and Paroedura picta Species Groups.

We present a comparative chromosome study of several taxa of the Malagasy ground geckos of the Paroedura bastardi and P. picta species groups. We employed a preliminary molecular analysis using a trait of the mitochondrial 16S rRNA gene (of about 570 bp) to assess the taxonomic status of the samples studied and a cytogenetic analysis with standard karyotyping (5% Giemsa solution), silver staining (Ag-NOR staining) and sequential C-banding (C-banding + Giemsa and + fluorochromes). Our results show that all the taxa studied of the P. bastardi group (P. ibityensis, P. rennerae and P. cf. guibeae) have a similar karyotype composed of 2n = 34 chromosomes, with two metacentric pairs (1 and 3) and all other pairs being acrocentric. Chromosome diversification in the P. bastardi group was mainly linked to the diversification of heteromorphic sex chromosome systems (ZZ/ZW) in P. ibityensis and P. rennerae, while no heteromorphic sex chromosome pair was found in P. cf. guibeae. The two taxa investigated of the P. picta species group (here named P. picta and P. cf. picta based on molecular data) showed the same chromosome number of 2n = 36, mostly acrocentric elements, but differed in the number of metacentric elements, probably as a result of an inversion at chromosome pair 2. We highlight that the genus Paroedura is characterized by the independent diversification of heterogametic sex chromosomes in different evolutionary lineages and, similarly to other phylogenetically related gecko genera, by a progressive formation of a biarmed element by means of tandem fusions and inversions of distinct pairs.

Identification and genetic analysis of a pervasive 'needle-eye' sperm phenotype in Drosophila sterile hybrid males.

Interspecies hybrid sterility has been extensively studied, especially in the genus Drosophila. Hybrid sterility is more often found in the heterogametic (XY or ZW) sex, a trend called Haldane's rule. Although this phenomenon is pervasive, identification of a common genetic mechanism remains elusive, with modest support found for a range of potential theories. Here, we identify a single precise morphological phenotype, which we call 'needle-eye sperm', that is associated with hybrid sterility in three separate species pairs that span the Drosophila genus. The nature of the phenotype indicates a common point of meiotic failure in sterile hybrid males. We used 10 generations of backcross selection paired with whole-genome pooled sequencing to genetically map the regions underlying the needle-eye (NE) sperm phenotype. Surprisingly, the sterility phenotype was present in ~50% of males even after 10 generations of backcrossing, and only a single region of the X chromosome was associated with sterility in one direction of backcross. Owing to the common phenotype among sterile male hybrids, and the strong effect of individual loci, further exploration of these findings may identify a universal mechanism for the evolution of hybrid sterility.

Evidence that genetic drift not adaptation drives fast-Z and large-Z effects in Ficedula flycatchers.

The sex chromosomes have been hypothesized to play a key role in driving adaptation and speciation across many taxa. The reason for this is thought to be the hemizygosity of the heteromorphic part of sex chromosomes in the heterogametic sex, which exposes recessive mutations to natural and sexual selection. The exposure of recessive beneficial mutations increases their rate of fixation on the sex chromosomes, which results in a faster rate of evolution. In addition, genetic incompatibilities between sex-linked loci are exposed faster in the genomic background of hybrids of divergent lineages, which makes sex chromosomes contribute disproportionately to reproductive isolation. However, in birds, which show a Z/W sex determination system, the role of adaptation versus genetic drift as the driving force of the faster differentiation of the Z chromosome (fast-Z effect) and the disproportionate role of the Z chromosome in reproductive isolation (large-Z effect) are still debated. Here, we address this debate in the bird genus Ficedula flycatchers based on population-level whole-genome sequencing data of six species. Our analysis provides evidence for both faster lineage sorting and reduced gene flow on the Z chromosome than the autosomes. However, these patterns appear to be driven primarily by the increased role of genetic drift on the Z chromosome, rather than an increased rate of adaptive evolution. Genomic scans of selective sweeps and fixed differences in fact suggest a reduced action of positive selection on the Z chromosome.

Understanding the genetic sex-determining mechanism in Hyla eximia treefrog inferred from H-Y antigen.

Genetic sex-determining mechanisms have been extensively elucidated in mammals; however, the sex chromosomes, sex-determining genes, and gene regulatory networks involved in sex differentiation remain poorly understood in amphibians. In this study, we investigated the sex-determining mechanism in the Hyla eximia treefrog based on karyotypic analysis and identification of H-Y antigen, a sex-linked peptide that is present in the gonads of the heterogametic sex (XY or ZW) in all vertebrates. Results show a diploid chromosome number 2n = 24 with homomorphic sex chromosomes. The heterogametic sex, ZW-female, were hypothesized based on H-Y antigen mRNA expression in female gonads (24,ZZ/24,ZW). The treefrog H-Y peptide exhibited a high percentage of identity with other vertebrate sequences uploaded to GenBank database. To obtain gene expression profiles, we also obtained the coding sequence of the housekeeping Actb gene. High H-Y antigen expression levels were further confirmed in ovaries using real-time polymerase chain reaction (RT-PCR) during non-breeding season, we noted a decrease in the expression of the H-Y antigen during breeding season. This study provides evidence that sex hormones might suppress H-Y antigen expression in the gonads of heterogametic females 24,ZW during the breeding season. These findings suggest that H-Y gene expression is a well-suited model for studying heterogametic sex by comparing the male and female gonads.

Pericentromeric recombination suppression and the ‘large X effect’ in plants

X chromosome was reported to be a major contributor to isolation between closely related species—the ‘large X’ effect (LXE). The causes of LXE are not clear, but the leading theory is that it is caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. However, the LXE was also reported in species with relatively recently evolved sex chromosomes where Y chromosome is not completely degenerate and X-linked genes are not hemizygous, such as the plant Silene latifolia. Recent genome sequencing and detailed genetic mapping in this species revealed a massive (> 330 Mb) non- or rarely-recombining pericentromeric region on the X chromosome (Xpr) that comprises ~ 90% of the chromosome and over 13% of the entire genome. If any of the Xpr genes are involved in species incompatibilities, this would oppose interspecific gene flow for other genes tightly linked in the Xpr. Here we test the hypothesis that the previously reported LXE in S. latifolia is caused by the lack of recombination on most of the X chromosome. Based on genome-wide analysis of DNA polymorphism and gene expression in S. latifolia and its close cross-compatible relative S. dioica, we report that the rarely-recombining regions represent a significant barrier for interspecific gene flow. We found little evidence for any additional factors contributing to the LXE, suggesting that extensive pericentromeric recombination suppression on the X-chromosome is the major if not the only cause of the LXE in S. latifolia and S. dioica.

An R-based tool for identifying sex-linked markers from restriction site-associated DNA sequencing with applications to elasmobranch conservation

Identifying sex-linked markers from genomic data has both theoretical and applied importance, especially in conservation. Yet, few methods and tools exist to detect such markers from Restriction-site-Associated DNA sequencing reads and even fewer tools can identify sex-linked markers from existing genotyped data. Here, we describe a new R function that can identify sex-linked markers in species with partially non-recombining sex chromosomes. We test the accuracy and speed of our function with an example dataset from a species of conservation concern, the White Shark, Carcharodon carcharias. We further compare our method against other approaches and find that our method detects more sex-linked markers that can be reliably mapped to reference genomes. Overall, we provide a conservation and fisheries-relevant tool that can reliably and efficiently assign sex from genetic data in species with a heterogametic sex and we demonstrate its utility by developing a sex-identification PCR test for White Sharks.

Bridging the cytogenetic gap in Trichoptera (Insecta): first karyotypic data on Neotropical species and insights into chromosomal evolution in caddisflies

Abstract Trichoptera are a diverse group of insects with aerial adults and aquatic immature stages. Despite their importance in freshwater environments, fundamental aspects of their biology are unknown, and no chromosomal studies have been performed in Neotropical species. The aim of this study was to provide the first cytogenetic analysis of four Trichoptera species from the Neotropics. We analysed the meiotic development and chromosome behaviour in Smicridea (Rhyacophylax) pampeana Flint (Annulipalpia: Hydropsychidae), Marilia flexuosa Ulmer (Integripalpia: Odontoceridae), Triplectides misionensis Holzenthal (Integripalpia: Leptoceridae), and Grumicha grumicha (Vallot) (Integripalpia: Sericostomatidae) by conventional cytogenetic procedures. The chromosome numbers are 2n = 31/32 (female/male) in S. (R.) pampeana, 2n = 57 (female) in M. flexuosa, 2n = 47 (female) in T. misionensis, and 2n = 35 (female) in G. grumicha. All four species have a simple sex chromosome system Z/ZZ (female/male). Females are the heterogametic sex, and their meiosis is achiasmatic. Our results together with available cytogenetic data provide more information on the karyology of Trichoptera and contribute to the current scientific knowledge of the possible mechanisms involved in chromosomal evolution. Based on all the evidence, we propose the existence of possible positive relationships between biological traits, ecological strategies, and cytogenetic features in Trichoptera.

U2 and U4 snDNA Comparative Chromosomal Mapping in the Neotropical Fish Genera Apareiodon and Parodon (Characiformes: Parodontidae).

Small nuclear DNA (snDNA) are valuable cytogenetic markers for comparative studies in chromosome evolution because different distribution patterns were found among species. Parodontidae, a Neotropical fish family, is known to have female heterogametic sex chromosome systems in some species. The U2 and U4 snDNA sites have been found to be involved in Z and W chromosome differentiation in Apareiodon sp., Apareiodon affinis, and Parodon hilarii. However, few studies have evaluated snDNA sites as propulsors of chromosome diversification among closely related fish species. In this study, we investigated the distribution of U2 and U4 snDNA clusters in the chromosomes of 10 populations/species belonging to Apareiodon and Parodon, aiming to identify chromosomal homeologies or diversification. In situ localization data revealed a submetacentric pair carrying the U2 snDNA site among the populations/species analyzed. Furthermore, all studied species demonstrated homeology in the location of U4 snDNA cluster in the proximal region of metacentric pair 1, besides an additional signal showing up with a divergence in Apareiodon. Comparative chromosomal mapping of U4 snDNA also helped to reinforce the proposal of the ZZ/ZW1W2 sex chromosome system origin in an A. affinis population. According to cytogenetic data, the study corroborates the diversification in Parodontidae paired species with uncertain taxonomy.

Sex Determination and Male Differentiation in Southern Swordtail Fishes: Evaluation from an Evolutionary Perspective

Southern swordtail fishes, which belong to the viviparous teleosts called Xiphophorus, are unique models for studies of evolution of sex chromosomes. Monofactorial sex-determining systems, with either the male or the female being the heterogametic sex, as well as sex determination involving more than two sex chromosomes, are found in swordtails and related species. Some swordtail species seem to have originated by crossing between two closely related species. Although the sword has disappeared in many Xiphophorus species during evolution, females of non-sworded species still prefer sworded males, demonstrating a discrepancy between natural and sexual selection. Natural sex change has not been documented sufficiently convincingly in swordtails, but, at least in some subspecies, two or more male phenotypes exist. In a laboratory experiment performed for over 30 years, it has been observed that sex-determining genes may be translocated from one chromosome to another in hybrids of these evolutionary young species. While the factors suggested to play central roles in sex determination and differentiation, e.g., Dmrt1 and AMH, are highly conserved during evolution, several master determining factors have been detected in teleosts. Endocrine-induced sex reversal has been demonstrated in the guppy Poecilia reticulata, another viviparous fish. In swordtails (X. helleri), endocrine disruptors such as nonylphenol and bisphenol A may cause testis cell degeneration and the inhibition of spermatogenesis. Furthermore, swordtails are very easy to breed in freshwater aquaria and, therefore, may be good models for studying the factors influencing sex determination and male differentiation.

A novel qPCR-based technique for identifying avian sex: An illustration within embryonic craniofacial bone.

Sex is a biological variable important to consider in all biomedical experiments. However, doing so in avian embryos can be challenging as sex can be morphologically indistinguishable. Unlike humans, female birds are the heterogametic sex with Z and W sex chromosomes. The female-specific W chromosome has previously been identified in chick using a species-specific polymerase chain reaction (PCR) technique. We developed a novel reverse transcription quantitative PCR (RT-qPCR) technique that amplifies the W chromosome gene histidine triad nucleotide-binding protein W (HINTW) in chick, quail, and duck. Accuracy of the HINTW RT-qPCR primer set was confirmed in all three species using species-specific PCR, including a novel quail-specific HINTW PCR primer set. Bone development-related gene expression was then analyzed by sex in embryonic lower jaws of duck and quail, as adult duck beak size is known to be sexually dimorphic while quail beak size is not. Trends toward sex differences were found in duck gene expression but not in quail, as expected. With these novel RT-qPCR and PCR embryo sexing methods, sex of chick, quail, and duck embryos can now be assessed by either/both RNA and DNA, which facilitates analysis of sex as a biological variable in studies using these model organisms.

Assembly of female and male hihi genomes (stitchbird; Notiomystis cincta) enables characterization of the W chromosome and resources for conservation genomics.

A high-quality reference genome can be a valuable resource for threatened species by providing a foundation to assess their evolutionary potential to adapt to future pressures such as environmental change. We assembled the genome of a female hihi (Notiomysits cincta), a threatened passerine bird endemic to Aotearoa New Zealand. The assembled genome is 1.06 Gb, and is of high quality and highly contiguous, with a contig N50 of 7.0 Mb, estimated QV of 44 and a BUSCO completeness of 96.8%. A male assembly of comparable quality was generated in parallel. A population linkage map was used to scaffold the autosomal contigs into chromosomes. Female and male sequence coverage and comparative genomics analyses were used to identify Z-, and W-linked contigs. In total, 94.6% of the assembly length was assigned to putative nuclear chromosome scaffolds. Native DNA methylation was highly correlated between sexes, with the W chromosome contigs more highly methylated than autosomal chromosomes and Z contigs. 43 differentially methylated regions were identified, and these may represent interesting candidates for the establishment or maintenance of sex differences. By generating a high-quality reference assembly of the heterogametic sex, we have created a resource that enables characterization of genome-wide diversity and facilitates the investigation of female-specific evolutionary processes. The reference genomes will form the basis for fine-scale assessment of the impacts of low genetic diversity and inbreeding on the adaptive potential of the species and will therefore enable tailored and informed conservation management of this threatened taonga (treasured) species.

A Test of Haldane's Rule in Neodiprion Sawflies and Implications for the Evolution of Postzygotic Isolation in Haplodiploids.

AbstractHaldane's rule-a pattern in which hybrid sterility or inviability is observed in the heterogametic sex of an interspecific cross-is one of the most widely obeyed rules in nature. Because inheritance patterns are similar for sex chromosomes and haplodiploid genomes, Haldane's rule may apply to haplodiploid taxa, predicting that haploid male hybrids will evolve sterility or inviability before diploid female hybrids. However, there are several genetic and evolutionary mechanisms that may reduce the tendency of haplodiploids to obey Haldane's rule. Currently, there are insufficient data from haplodiploids to determine how frequently they adhere to Haldane's rule. To help fill this gap, we crossed a pair of haplodiploid hymenopteran species (Neodiprion lecontei and Neodiprion pinetum) and evaluated the viability and fertility of female and male hybrids. Despite considerable divergence, we found no evidence of reduced fertility in hybrids of either sex, consistent with the hypothesis that hybrid sterility evolves slowly in haplodiploids. For viability, we found a pattern opposite to that of Haldane's rule: hybrid females, but not males, had reduced viability. This reduction was most pronounced in one direction of the cross, possibly due to a cytoplasmic-nuclear incompatibility. We also found evidence of extrinsic postzygotic isolation in hybrids of both sexes, raising the possibility that this form or reproductive isolation tends to emerge early in speciation in host-specialized insects. Our work emphasizes the need for more studies on reproductive isolation in haplodiploids, which are abundant in nature but underrepresented in the speciation literature.

Identification and Genomic Localization of Autosomal sdY Locus in a Population of Atlantic Salmon (Salmo salar).

The determination of sex in salmonid fishes is controlled by genetic mechanisms, with males being the heterogametic sex. The master sex-determining gene, the sexually dimorphic gene on the Y chromosome (sdY), is a conserved gene across various salmonid species. Nevertheless, variations in the genomic location of sdY have been observed both within and between species. Furthermore, different studies have reported discordances in the association between the sdY and the phenotypic gender. While some males seem to lack this locus, there have been reports of females carrying sdY. Although the exact reasons behind this discordance remain under investigation, some recent studies have proposed the existence of an autosomal, non-functional copy of sdY as a potential cause. In this study, we confirmed the presence of this autosomal sdY in the SalmoBreed strain of Atlantic salmon using a genotyping platform through a novel approach that allows for high-throughput screening of a large number of individuals. We further characterized the segregation profile of this locus across families and found the ratio of genetically assigned female-to-male progeny to be in accordance with the expected profile of a single autosomal sdY locus. Additionally, our mapping efforts localized this locus to chromosome 3 and suggested a putative copy on chromosome 6.

Hybrid breakdown in male reproduction between recently diverged Drosophila melanogaster populations has a complex and variable genetic architecture.

Secondary contact between formerly isolated populations may result in hybrid breakdown, in which untested allelic combinations in hybrids are maladaptive and limit genetic exchange. Studying early-stage reproductive isolation may yield key insights into the genetic architectures and evolutionary forces underlying the first steps toward speciation. Here, we leverage the recent worldwide expansion of Drosophila melanogaster to test for hybrid breakdown between populations that diverged within the last 13,000 years. We found clear evidence for hybrid breakdown in male reproduction, but not female reproduction or viability, supporting the prediction that hybrid breakdown affects the heterogametic sex first. The frequency of non-reproducing F2 males varied among different crosses involving the same southern African and European populations, as did the qualitative effect of cross direction, implying a genetically variable basis of hybrid breakdown and a role for uniparentally inherited factors. The levels of breakdown observed in F2 males were not recapitulated in backcrossed individuals, consistent with the existence of incompatibilities with at least three partners. Thus, some of the very first steps toward reproductive isolation could involve incompatibilities with complex and variable genetic architectures. Collectively, our findings emphasize this system's potential for future studies on the genetic and organismal basis of early-stage reproductive isolation.

Heterochiasmy and Sex Chromosome Evolution in Silene

The evolution of a non-recombining sex-specific region is a key step in sex chromosome evolution. Suppression of recombination between the (proto-) X- and Y-chromosomes in male meiosis creates a non-recombining Y-linked region (NRY), while the X-chromosome continues to recombine in females. Lack of recombination in the NRY defines its main properties-genetic degeneration and accumulation of repetitive DNA, making X and Y chromosomes very different from each other. How and why recombination suppression on sex chromosomes evolves remains controversial. A strong difference in recombination rates between the sexes (heterochiasmy) can facilitate or even cause recombination suppression. In the extreme case-complete lack of recombination in the heterogametic sex (achiasmy)-the entire sex-specific chromosome is automatically non-recombining. In this study, I analyse sex-specific recombination rates in a dioecious plant Silene latifolia (Caryophyllaceae), which evolved separate sexes and sex chromosomes ~11 million years ago. I reconstruct high-density RNAseq-based genetic maps including over five thousand genic markers for the two sexes separately. The comparison of the male and female maps reveals only modest heterochiasmy across the genome, with the exception of the sex chromosomes, where recombination is suppressed in males. This indicates that heterochiasmy likely played only a minor, if any, role in NRY evolution in S. latifolia, as recombination suppression is specific to NRY rather than to the entire genome in males. Other mechanisms such as structural rearrangements and/or epigenetic modifications were likely involved, and comparative genome analysis and genetic mapping in multiple Silene species will help to shed light on the mechanism(s) of recombination suppression that led to the evolution of sex chromosomes.

Evolutionary History of the Poecilia picta Sex Chromosomes.

The degree of divergence between the sex chromosomes is not always proportional to their age. In poeciliids, four closely related species all exhibit a male heterogametic sex chromosome system on the same linkage group, yet show a remarkable diversity in X and Y divergence. In Poecilia reticulata and P. wingei, the sex chromosomes remain homomorphic, yet P. picta and P. parae have a highly degraded Y chromosome. To test alternative theories about the origin of their sex chromosomes, we used a combination of pedigrees and RNA-seq data from P. picta families in conjunction with DNA-seq data collected from P. reticulata, P. wingei, P. parae, and P. picta. Phylogenetic clustering analysis of X and Y orthologs, identified through segregation patterns, and their orthologous sequences in closely related species demonstrates a similar time of origin for both the P. picta and P. reticulata sex chromosomes. We next used k-mer analysis to identify shared ancestral Y sequence across all four species, suggesting a single origin to the sex chromosome system in this group. Together, our results provide key insights into the origin and evolution of the poeciliid Y chromosome and illustrate that the rate of sex chromosome divergence is often highly heterogenous, even over relatively short evolutionary time frames.

Recombination and selection against introgressed DNA.

Introgressed DNA is often deleterious at many loci in the recipient species' genome, and is therefore purged by selection. Here, we use mathematical modeling and whole-genome simulations to study the influence of recombination on this process. We find that aggregate recombination controls the genome-wide rate of purging in the early generations after admixture, when purging is most rapid. Aggregate recombination is influenced by the number of chromosomes and heterogeneity in their size, and by the number of crossovers and their locations along chromosomes. A comparative prediction is that species with fewer chromosomes should purge introgressed ancestry more profoundly, and should therefore exhibit weaker genomic signals of historical introgression. Turning to within-genome patterns, we show that, in species with autosomal recombination in both sexes, more purging is expected on sex chromosomes than autosomes, all else equal. The opposite prediction holds for species without autosomal recombination in the heterogametic sex. Finally, positive correlations between recombination rate and introgressed ancestry have recently been observed within the genomes of several species. We show that these correlations are likely driven not by recombination's effect in unlinking neutral from deleterious introgressed alleles, but by recombination's effect on the rate of purging of deleterious introgressed alleles themselves.