Haldane's Rule Research Articles

System drift and speciation.

Even if a species' phenotype does not change over evolutionary time, the underlying mechanism may change, as distinct molecular pathways can realize identical phenotypes. Here we use linear system theory to explore the consequences of this idea, describing how a gene network underlying a conserved phenotype evolves, as the genetic drift of small changes to these molecular pathways causes a population to explore the set of mechanisms with identical phenotypes. To do this, we model an organism's internal state as a linear system of differential equations for which the environment provides input and the phenotype is the output, in which context there exists an exact characterization of the set of all mechanisms that give the same input‐output relationship. This characterization implies that selectively neutral directions in genotype space should be common and that the evolutionary exploration of these distinct but equivalent mechanisms can lead to the reproductive incompatibility of independently evolving populations. This evolutionary exploration, or system drift, is expected to proceed at a rate proportional to the amount of intrapopulation genetic variation divided by the effective population size (Ne). At biologically reasonable parameter values this could lead to substantial interpopulation incompatibility, and thus speciation, on a time scale of Ne generations. This model also naturally predicts Haldane's rule, thus providing a concrete explanation of why heterogametic hybrids tend to be disrupted more often than homogametes during the early stages of speciation.

Asymmetric viability in reciprocal crosses of zebrafish Danio rerio and pearl danio Danio albolineatus.

Interspecies hybrids have long been studied to further understanding of speciation. Reciprocal crosses sometimes have asymmetric viability, a phenomenon termed 'Darwin's corollary to Haldane's rule'. It has been proposed that this asymmetry is caused by Dobzhansky-Muller incompatibilities between nuclear genes and cytoplasmic factors (e.g., maternal transcripts, mitochondrial genome). The molecular basis of this hypothesis has received little empirical investigation, presumably due to the lack of an appropriate model system. We report a case of extreme asymmetry in viability between reciprocal hybrids of zebrafish Danio rerio and pearl danio Danio albolineatus. Hybrids from D. rerio females × D. albolineatus males (n=4 crosses) were viable, with 83.2 ± 9.6% surviving from fertilization to 5 days post-fertilization (dpf) and 80.1 ± 14.4% surviving from 5 to 21 dpf. Hybrids from D. albolineatus females × D. rerio males (n=6 crosses) were inviable after embryonic development. These hybrids developed pericardial oedema at 1dpf and only 37.2 ± 18.0% survived from fertilization to 5dpf. Of the 595 larvae alive at 5dpf, only one juvenile with stunted growth survived to 21 dpf. We propose that given the resources available for the D. rerio model system and the strong asymmetry in viability between reciprocal crosses, these hybrids will allow investigation of the molecular basis for Darwin's corollary to Haldane's rule.

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities.

It is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here, we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of greater than 55% compared to the genome-wide density of less than 10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesize that the avian W chromosome acts as a refugium for active ERVs, probably leading to female-biased mutational load that may influence female physiology similar to the ‘toxic-Y’ effect in Drosophila males. Furthermore, Haldane's rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane's rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage.This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Haldane’s duel: intragenomic conflict, selfish Y chromosomes and speciation

Haldane's rule, which states that the heterogametic sex (XY or ZW females) fares more poorly in interspecific hybrids, is generally attributed to absence of one of the two species' X/Z chromosomes. However, Haldane's rule is also observed in mouse placentas despite paternal X silencing. This pattern could reflect Y chromosomes having evolved to promote growth due to maternal-paternal conflict. If so, balanced sex investment arises from a complex intra- and intergenomic duel.

Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone.

The exploration of hybrid zones and the intergenomic conflicts exposed through hybridization provide windows into the processes of divergence and speciation. Sex chromosomes and mitonuclear incompatibilities have strong associations with the genetics of hybrid dysfunction. In ZW sex-determining systems, maternal co-inheritance of the mitochondrial and W chromosomes immediately exposes incompatibilities between these maternal contributions of one species and the Z chromosome of another. We analyze mitochondrial and Z chromosome admixture in the long-tailed finch (Poephila acuticauda) of Australia, where hybridizing subspecies differ prominently in Z chromosome genotype and in bill color, yet the respective centers of geographic admixture for these two traits are offset by 350 km. We report two well-defined mitochondrial clades that diverged ∼0.5 million years ago. Mitochondrial contact is geographically co-located within a hybrid zone of Z chromosome admixture and is displaced from bill color admixture by nearly 400 km. Consistent with Haldane's rule expectations, hybrid zone females are significantly less likely than males to carry an admixed Z chromosome or have mismatched Z-mitochondrial genotypes. Furthermore, there are significantly fewer than expected mitonuclear mismatches in hybrid zone females and paternal backcross males. Results suggest a potential for mitonuclear/sex chromosome incompatibilities in the emergence of reproductive isolation in this system.

Pleistocene divergence in the absence of gene flow among populations of a viviparous reptile with intraspecific variation in sex determination.

Polymorphisms can lead to genetic isolation if there is differential mating success among conspecifics divergent for a trait. Polymorphism for sex‐determining system may fall into this category, given strong selection for the production of viable males and females and the low success of heterogametic hybrids when sex chromosomes differ (Haldane's rule). Here we investigated whether populations exhibiting polymorphism for sex determination are genetically isolated, using the viviparous snow skink Carinascincus ocellatus. While a comparatively high elevation population has genotypic sex determination, in a lower elevation population there is an additional temperature component to sex determination. Based on 11,107 SNP markers, these populations appear genetically isolated. “Isolation with Migration” analysis also suggests these populations diverged in the absence of gene flow, across a period encompassing multiple Pleistocene glaciations and likely greater geographic proximity of populations. However, further experiments are required to establish whether genetic isolation may be a cause or consequence of differences in sex determination. Given the influence of temperature on sex in one lineage, we also discuss the implications for the persistence of this polymorphism under climate change.

Chromosomal evolution in Raphicerus antelope suggests divergent X chromosomes may drive speciation through females, rather than males, contrary to Haldane's rule

Chromosome structural change has long been considered important in the evolution of post-zygotic reproductive isolation. The premise that karyotypic variation can serve as a possible barrier to gene flow is founded on the expectation that heterozygotes for structurally distinct chromosomal forms would be partially sterile (negatively heterotic) or show reduced recombination. We report the outcome of a detailed comparative molecular cytogenetic study of three antelope species, genus Raphicerus, that have undergone a rapid radiation. The species are largely conserved with respect to their euchromatic regions but the X chromosomes, in marked contrast, show distinct patterns of heterochromatic amplification and localization of repeats that have occurred independently in each lineage. We argue a novel hypothesis that postulates that the expansion of heterochromatic blocks in the homogametic sex can, with certain conditions, contribute to post-zygotic isolation. i.e., female hybrid incompatibility, the converse of Haldane’s rule. This is based on the expectation that hybrids incur a selective disadvantage due to impaired meiosis resulting from the meiotic checkpoint network’s surveillance of the asymmetric expansions of heterochromatic blocks in the homogametic sex. Asynapsis of these heterochromatic regions would result in meiotic silencing of unsynapsed chromatin and, if this persists, germline apoptosis and female infertility.

Haldane's rule in the placenta: Sex‐biased misregulation of the Kcnq1 imprinting cluster in hybrid mice

Hybrid phenotypes that contribute to postzygotic reproductive isolation often exhibit pronounced asymmetry, both between reciprocal crosses and between the sexes in accordance with Haldane's rule. Inviability in mammalian hybrids is associated with parent-of-origin placental growth abnormalities for which misregulation of imprinted gene (IGs) is the leading candidate mechanism. However, direct evidence for the involvement of IGs in hybrid growth dysplasia is limited. We used transcriptome and reduced representation bisulfite sequencing to conduct the first genome-scale assessment of the contribution of IGs to parent-of-origin placental growth dysplasia in the cross between the house mouse (Mus musculus domesticus) and the Algerian mouse (Mus spretus). IGs with transgressive expression and methylation were concentrated in the Kcnq1 cluster, which contains causal genes for prenatal growth abnormalities in mice and humans. Hypermethylation of the cluster's imprinting control region, and consequent misexpression of the genes Phlda2 and Ascl2, is a strong candidate mechanism for transgressive placental undergrowth. Transgressive placental and gene regulatory phenotypes, including expression and methylation in the Kcnq1 cluster, were more extreme in hybrid males. Although consistent with Haldane's rule, male-biased defects are unexpected in rodent placenta because the X-chromosome is effectively hemizygous in both sexes. In search of an explanation, we found evidence of leaky imprinted (paternal) X-chromosome inactivation in hybrid female placenta, an epigenetic disturbance that may buffer females from the effects of X-linked incompatibilities to which males are fully exposed. Sex differences in chromatin structure on the X and sex-biased maternal effects are nonmutually exclusive alternative explanations for adherence to Haldane's rule in hybrid placenta. The results of this study contribute to understanding the genetic basis of hybrid inviability in mammals, and the role of IGs in speciation.

Male hybrid sterility in the cattle-yak and other bovines: a review.

Hybridization is important for both animal breeders attempting to fix new phenotypic traits and researchers trying to unravel the mechanism of reproductive barriers in hybrid species and the process of speciation. In interspecies animal hybrids, gains made in terms of adaptation to environmental conditions and hybrid vigor may be offset by reduced fertility or sterility. Bovine hybrids exhibit remarkable hybrid vigor compared to their parents. However, the F1 male hybrid exhibits sterility, whereas the female is fertile. This male-biased sterility is consistent with the Haldane rule where heterogametic sex is preferentially rare, absent, or sterile in the progeny of two different species. The obstacle of fixing favorable traits and passing them to subsequent generations due to the male sterility is a major setback in improving the reproductive potential of bovines through hybridization. Multiperspective approaches such as molecular genetics, proteomics, transcriptomics, physiology, and endocrinology have been used by several researchers over the past decade in an attempt to unravel the potential mechanisms underlying male hybrid sterility. However, the mechanism of sterility in the hybrid male is still not completely unravelled. This review seeks to provide an update of the mechanisms of the sterility in the cattle-yak and other bovines.

Hybridization and introgression between toads with different sex chromosome systems

The growing interest in the lability of sex determination in non‐model vertebrates such as amphibians and fishes has revealed high rates of sex chromosome turnovers among closely related species of the same clade. Can such lineages hybridize and admix with different sex‐determining systems, or could the changes have precipitated their speciation? We addressed these questions in incipient species of toads (Bufonidae), where we identified a heterogametic transition and characterized their hybrid zone with genome‐wide markers (RADseq). Adult and sibship data confirmed that the common toad B. bufo is female heterogametic (ZW), while its sister species the spined toad B. spinosus is male heterogametic (XY). Analysis of a fine scale transect across their parapatric ranges in southeastern France unveiled a narrow tension zone (∼10 km), with asymmetric mitochondrial and nuclear admixture over hundreds of kilometers southward and northward, respectively. The geographic extent of introgression is consistent with an expansion of B. spinosus across B. bufo’s former ranges in Mediterranean France, as also suggested by species distribution models. However, widespread cyto‐nuclear discordances (B. spinosus backrosses carrying B. bufo mtDNA) run against predictions from the dominance effects of Haldane's rule, perhaps because Y and W heterogametologs are not degenerated. Common and spined toads can thus successfully cross‐breed despite fundamental differences in their sex determination mechanisms, but remain partially separated by reproductive barriers. Whether and how the interactions of their XY and ZW genes contribute to these barriers shall provide novel insights on the debated role of labile sex chromosomes in speciation.

A mitochondrial genetic divergence proxy predicts the reproductive compatibility of mammalian hybrids.

Numerous pairs of evolutionarily divergent mammalian species have been shown to produce hybrid offspring. In some cases, F1 hybrids are able to produce F2s through matings with F1s. In other instances, the hybrids are only able to produce offspring themselves through backcrosses with a parent species owing to unisexual sterility (Haldane's Rule). Here, we explicitly tested whether genetic distance, computed from mitochondrial and nuclear genes, can be used as a proxy to predict the relative fertility of the hybrid offspring resulting from matings between species of terrestrial mammals. We assessed the proxy's predictive power using a well-characterized felid hybrid system, and applied it to modern and ancient hominins. Our results revealed a small overlap in mitochondrial genetic distance values that distinguish species pairs whose calculated distances fall within two categories: those whose hybrid offspring follow Haldane's Rule, and those whose hybrid F1 offspring can produce F2s. The strong correlation between genetic distance and hybrid fertility demonstrated here suggests that this proxy can be employed to predict whether the hybrid offspring of two mammalian species will follow Haldane's Rule.

Hybridization in human evolution: Insights from other organisms.

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex-differences in behavior, Haldane's rule and the large X-effect, and transgressive phenotypic variation.

Phenotypic effects of the Y chromosome are variable and structured in hybrids among house mouse recombinant lines.

Hybrid zones between divergent populations sieve genomes into blocks that introgress across the zone, and blocks that do not, depending on selection between interacting genes. Consistent with Haldane's rule, the Y chromosome has been considered counterselected and hence not to introgress across the European house mouse hybrid zone. However, recent studies detected massive invasion of M. m. musculus Y chromosomes into M. m. domesticus territory. To understand mechanisms facilitating Y spread, we created 31 recombinant lines from eight wild‐derived strains representing four localities within the two mouse subspecies. These lines were reciprocally crossed and resulting F1 hybrid males scored for five phenotypic traits associated with male fitness. Molecular analyses of 51 Y‐linked SNPs attributed ~50% of genetic variation to differences between the subspecies and 8% to differentiation within both taxa. A striking proportion, 21% (frequencies of sperm head abnormalities) and 42% (frequencies of sperm tail dissociations), of phenotypic variation was explained by geographic Y chromosome variants. Our crossing design allowed this explanatory power to be examined across a hierarchical scale from subspecific to local intrastrain effects. We found that divergence and variation were expressed diversely in different phenotypic traits and varied across the whole hierarchical scale. This finding adds another dimension of complexity to studies of Y introgression not only across the house mouse hybrid zone but potentially also in other contact zones.

Introgression across Hybrid Zones Is Not Mediated by Large X-Effects in Green Toads with Undifferentiated Sex Chromosomes.

Divergence between incipient species remains an incompletely understood process. Hybrid zones provide great research potential, reflecting natural organismal genomic interactions and gene evolution in a variety of recombinants over generations. While sex chromosomes are known evolutionary drivers of reproductive isolation, empirical population genetics has mostly examined species with heteromorphic sex chromosomes. We recently reported restricted introgression at sex-linked markers in an amphibian system with homomorphic sex chromosomes (Hyla), consistent with a large X-effect, designating a greater role of sex chromosomes in driving hybrid incompatibilities. Here, using a similar approach, we examined two hybrid zones of Palearctic green toads (Bufo viridis subgroup), involving several lineages that arose at different times and form secondary contacts. We find no evidence for differential introgression of sex-linked versus autosomal markers across both zones. This absence of large X-effects in Bufo indicates that, unlike in Hyla, hybrid incompatibilities may not result from the faster-heterogametic sex and faster-male aspects of Haldane's rule. The recent suppression of XY recombination in Hyla but not in Bufo may have driven greater divergence between Hyla sex chromosomes, causing stronger reproductive isolation. Alternatively, stronger linkage among Hyla's sex-linked markers could restrict introgression. We hypothesize that the degree of sex-specific recombination may condition the importance of homomorphic sex chromosomes in speciation.

Geographic patterns of postzygotic isolation between two closely related widespread dung fly species (Sepsis cynipseaandSepsis neocynipsea; Diptera: Sepsidae)

Identifying the contribution of pre‐ and postzygotic barriers to gene flow is a key goal of speciation research. The widespread dung fly species Sepsis cynipsea and Sepsis neocynipsea offer great potential for studying the speciation process over a range of opportunities for gene exchange within and across sister species (cross‐continental allopatry, continental parapatry and sympatry). We examined the role of postcopulatory isolating barriers by comparing female fecundity and egg‐to‐adult viability of F1 and F2 hybrids, as well as backcrosses of F1 hybrids with the parental species, via replicated crosses of sym‐, para‐ and allopatric populations. Egg‐to‐adult viability was strongly but not totally suppressed in hybrids, and offspring production approached nil in the F2 generation (hybrid breakdown), indicating yet unspecified intrinsic incompatibilities. Viable F1 hybrid offspring showed almost absolute male (the heterogametic sex) sterility while females remained largely fertile, in accordance with Haldane's rule. Hybridization between the two species in European areas of sympatry (Swiss Alps) indicated only minor reinforcement based on fecundity traits. Crossing geographically isolated European and North American S. neocynipsea showed similar albeit weaker isolating barriers that are most easily explained by random genetic drift. We conclude that in this system with a biogeographic continuum of reproductive barriers, speciation is mediated primarily by genetic drift following dispersal of flies over a wide (allopatric) geographic range, with some role of natural or sexual selection in incidental or direct reinforcement of incompatibility mechanisms in areas of European sympatry. S(ubs)pecies status of continental S. neocynipsea appears warranted.

Evaluating genomic signatures of "the large X-effect" during complex speciation.

The ubiquity of the "two rules of speciation"-Haldane's rule and the large X-effect-implies a general, special role for sex chromosomes in the evolution of intrinsic postzygotic reproductive isolation. The recent proliferation of genome-scale analyses has revealed two further general observations: (a) complex speciation involving some form of gene flow is not uncommon, and (b) sex chromosomes in male- and in female-heterogametic taxa tend to show elevated differentiation relative to autosomes. Together, these observations are consistent with speciation histories in which population genetic differentiation at autosomal loci is reduced by gene flow while natural selection against hybrid incompatibilities renders sex chromosomes relatively refractory to gene flow. Here, I summarize multilocus population genetic and population genomic evidence for greater differentiation on the X (or Z) vs. the autosomes and consider the possible causes. I review common population genetic circumstances involving no selection and/or no interspecific gene flow that are nevertheless expected to elevate differentiation on sex chromosomes relative to autosomes. I then review theory for why large X-effects exist for hybrid incompatibilities and, more generally, for loci mediating local adaptation. The observed levels of sex chromosome vs. autosomal differentiation, in many cases, appear consistent with simple explanations requiring neither large X-effects nor gene flow. Discerning signatures of large X-effects during complex speciation will therefore require analyses that go beyond chromosome-scale summaries of population genetic differentiation, explicitly test for differential introgression, and/or integrate experimental genetic data.

Dobzhansky-Muller incompatibilities, dominance drive, and sex-chromosome introgression at secondary contact zones: A simulation study.

Dobzhansky-Muller (DM) incompatibilities involving sex chromosomes have been proposed to account for Haldane's rule (lowered fitness among hybrid offspring of the heterogametic sex) as well as Darwin's corollary (asymmetric fitness costs with respect to the direction of the cross). We performed simulation studies of a hybrid zone to investigate the effects of different types of DM incompatibilities on cline widths and positions of sex-linked markers. From our simulations, X-Y incompatibilities generate steep clines for both X-linked and Y-linked markers; random effects may produce strong noise in cline center positions when migration is high relative to fitness costs, but X- and Y-centers always coincide strictly. X-autosome and Y-autosome incompatibilities also generate steep clines, but systematic shifts in cline centers occur when migration is high relative to selection, as a result of a dominance drive linked to Darwin's corollary. Interestingly, sex-linked genes always show farther introgression than the associated autosomal genes. We discuss ways of disentangling the potentially confounding effects of sex biases in migration, we compare our results to those of a few documented contact zones, and we stress the need to study independent replicates of the same contact zone.

Transgressive phenotypes and evidence of weak postzygotic isolation in F1 hybrids between closely related capuchino seedeaters.

Postzygotic reproductive isolation may become strong only once the process of speciation is in its advanced stages. For taxa in the early stages of speciation, prezygotic reproductive isolation barriers may play a predominant role in maintaining species boundaries. Here, we study the recent capuchino seedeater biological radiation, a group of highly sympatric species from the genus Sporophila that have diversified during the Pleistocene in Neotropical grasslands. Capuchinos can be diagnosed by adult male coloration patterns and song, two sets of characters known to contribute to pre-mating reproductive isolation. However, it remains unknown whether potzygotic incompatibilities contribute to maintaining species limits in this group. Here we use existing breeding records from captive individuals to test for patterns consistent with F1 inviability. We compare hatching success, fledging success, and the sex ratio at adulthood between conspecific and hybrid capuchino pairs. We observed a trend towards lower numbers of the heterogametic sex among adult hybrids, consistent Haldane's rule, but this was supported by only one of our statistical tests. Our study is the first to document hybrid male capuchino phenotypes based on known crosses. We observed phenotypes that were similar or intermediate to those of the parental species, as well as novel plumage patterns that have not been described in the wild. One cross produced a plumage pattern that has been observed at low frequencies in natural populations. We discuss the implications of our results for understanding the relative importance of the mechanisms of reproductive isolation in capuchino seedeaters.

Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes.

Linking intraspecificand interspecificdivergenceis an important challenge inspeciation research. X chromosomesare expected toevolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16 population transect of two closely related Australian cricket species,Teleogryllus commodusandT.oceanicus,covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane's rule, as hybrid females are sterile. We found no evidence of recentintrogression, despite the fact that the species coexist in overlapping habitats in the wild and interbreed in the laboratory. Putative X-linked loci showed greater differentiation between species compared with autosomal loci. However, population differentiation within species was unexpectedly lower on X-linked markers than autosomal markers, and relative X-to-autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex-biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex-linked genes in maintaining species boundaries in this system.

The two "rules of speciation" in species with young sex chromosomes.

The two "rules of speciation," Haldane's rule (HR) and the large-X effect (LXE), are thought to be caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. Thus, the reports of HR and the LXE in species with recently evolved non- or partially degenerate Y-chromosomes, such as Silene latifolia and its relatives, were surprising. Here, I argue that rapid species-specific degeneration of Y-linked genes and associated adjustment of expression of X-linked gametologs (dosage compensation) may lead to rapid evolution of sex-linked species incompatibilities. This process is likely to be too slow in species with old degenerate Y-chromosomes (e.g., in mammals), but Y-degeneration in species with young gene-rich sex chromosomes may be fast enough to play a significant role in speciation. To illustrate this point, I report the analysis of Y-degeneration and the associated evolution of gene expression on the X-chromosome of S.latifolia and Silene dioica, a close relative that shares the same recently evolved sex chromosomes. Despite the recent (≤1MY) divergence of the two species, ~7% of Y-linked genes have undergone degeneration in one but not the other species. This species-specific degeneration appears to drive faster expression divergence of X-linked genes, which may account for HR and the LXE reported for these species. Furthermore, I suggest that "exposure" of autosomal or sex-linked recessive species incompatibilities in the haploid plant gametophyte may mimic the presence of HR in plants. Both haploid expression and species-specific Y-degeneration need to receive more attention if we are to understand the role of these processes in speciation.