Mass of genes rather than master genes underlie the genomic architecture of amphibian speciation

The genetic architecture of speciation, i.e., how intrinsic genomic incompatibilities promote reproductive isolation (RI) between diverging lineages, is one of the best-kept secrets of evolution. To directly assess whether incompatibilities arise in a limited set of large-effect speciation genes, or in a multitude of loci, we examined the geographic and genomic landscapes of introgression across the hybrid zones of 41 pairs of frog and toad lineages in the Western Palearctic region. As the divergence between lineages increases, phylogeographic transitions progressively become narrower, and larger parts of the genome resist introgression. This suggests that anuran speciation proceeds through a gradual accumulation of multiple barrier loci scattered across the genome, which ultimately deplete hybrid fitness by intrinsic postzygotic isolation, with behavioral isolation being achieved only at later stages. Moreover, these loci were disproportionately sex linked in one group (Hyla) but not in others (Rana and Bufotes), implying that large X-effects are not necessarily a rule of speciation with undifferentiated sex chromosomes. The highly polygenic nature of RI and the lack of hemizygous X/Z chromosomes could explain why the speciation clock ticks slower in amphibians compared to other vertebrates. The clock-like dynamics of speciation combined with the analytical focus on hybrid zones offer perspectives for more standardized practices of species delimitation.

The Integrity of the HMR complex is necessary for centromeric binding and reproductive isolation in Drosophila

Postzygotic isolation by genomic conflict is a major cause for the formation of species. Despite its importance, the molecular mechanisms that result in the lethality of interspecies hybrids are still largely unclear. The genus Drosophila, which contains over 1600 different species, is one of the best characterized model systems to study these questions. We showed in the past that the expression levels of the two hybrid incompatibility factors Hmr and Lhr diverged in the two closely related Drosophila species, D. melanogaster and D. simulans, resulting in an increased level of both proteins in interspecies hybrids. The overexpression of the two proteins also leads to mitotic defects, a misregulation in the expression of transposable elements and decreased fertility in pure species. In this work, we describe a distinct six subunit protein complex containing HMR and LHR and analyse the effect of Hmr mutations on complex integrity and function. Our experiments suggest that HMR needs to bring together components of centromeric and pericentromeric chromatin to fulfil its physiological function and to cause hybrid male lethality.

Comparative transcriptomics between Drosophila mojavensis and D. arizonae reveals transgressive gene expression and underexpression of spermatogenesis-related genes in hybrid testes

Interspecific hybridization is a stressful condition that can lead to sterility and/or inviability through improper gene regulation in Drosophila species with a high divergence time. However, the extent of these abnormalities in hybrids of recently diverging species is not well known. Some studies have shown that in Drosophila, the mechanisms of postzygotic isolation may evolve more rapidly in males than in females and that the degree of viability and sterility is associated with the genetic distance between species. Here, we used transcriptomic comparisons between two Drosophila mojavensis subspecies and D. arizonae (repleta group, Drosophila) and identified greater differential gene expression in testes than in ovaries. We tested the hypothesis that the severity of the interspecies hybrid phenotype is associated with the degree of gene misregulation. We showed limited gene misregulation in fertile females and an increase in the amount of misregulation in males with more severe sterile phenotypes (motile vs. amotile sperm). In addition, for these hybrids, we identified candidate genes that were mostly associated with spermatogenesis dysfunction.

The Integrity of the Speciation Core Complex is necessary for centromeric binding and reproductive isolation in Drosophila

ABSTRACTPostzygotic isolation by genomic conflict is a major cause for the formation of species. Despite its importance, the molecular mechanisms that result in the lethality of interspecies hybrids are still largely unclear. The genus Drosophila, which contains over 1600 different species, is one of the best characterized model systems to study these questions. We showed in the past that the expression levels of the two hybrid incompatibility factors Hmr and Lhr diverged in the two closely related Drosophila species, D. melanogaster and D. simulans, resulting in an increased level of both proteins in interspecies hybrids. This overexpression leads to mitotic defects, a misregulation in the expression of transposable elements and a decreased fertility. In this work, we describe a distinct six subunit Speciation Core Complex (SCC) containing HMR and LHR and analyse the effect of Hmr mutations on complex function and integrity. Our experiments suggest that HMR acts as a bridging factor between centromeric chromatin and pericentromeric heterochromatin, which is required for both its physiological function and its ability to cause hybrid male lethality.

Asymmetric reinforcement in Lucania killifish: assessing reproductive isolation when both sexes choose

Reinforcement can occur when maladaptive hybridization in sympatry favors the evolution of conspecific preferences and target traits that promote behavioral isolation (BI). In many systems, enhanced BI is due to increased female preference for conspecifics. In others, BI is driven by male preference, and in other systems both sexes exert preferences. Some of these patterns can be attributed to classic sex-specific costs and benefits of preference. Alternatively, sex differences in conspecific preference can emerge due to asymmetric postzygotic isolation (e.g., hybrid offspring from female A × male B have lower fitness than hybrid offspring from female B × male A), which can lead to asymmetric BI (e.g., female A and male B are less likely to mate than female B and male A). Understanding reinforcement requires understanding how conspecific preferences evolve in sympatry. Yet, estimating conspecific preferences can be difficult when both sexes are choosy. In this study, we use Lucania killifish to test the hypothesis that patterns of reinforcement are driven by asymmetric postzygotic isolation between species. If true, we predicted that sympatric female Lucania goodei and sympatric male L. parva should have lower levels of BI compared with their sympatric counterparts, as they produce hybrid offspring with the highest fitness. To address the problem of measuring BI when both sexes are choosy, we inferred the contribution to BI of each partner using assays where one sex in the mating pair comes from an allopatric population with potentially low preference, whereas the other comes from a sympatric population with high preference. For one hybrid cross direction, we found that both female L. parva and male L. goodei have high contributions to BI in sympatry. In the other hybrid cross direction, we found that only female L. goodei contribute to BI. Sympatric male L. parva readily engaged in hybrid spawnings with allopatric L. goodei females. These results indicate that both asymmetric postzygotic isolation and the traditional sex-specific costs to preference likely affect the nature of selection on conspecific preferences and target traits.

Evolutionary dynamics of pre- and postzygotic reproductive isolation in cichlid fishes

Cichlid fishes are exceptionally species-rich, speciated at explosive rates and, hence, are a model system in speciation research. Yet, their reproductive isolating barriers have, so far, not been comprehensively studied. Here, we review current knowledge on pre- and postzygotic mechanisms in cichlids. While premating isolation is the norm in cichlids, its strength varies across lineages and with the geographical setting. Moreover, manipulations of ambient conditions tended to reduce assortative mating among closely related species, suggesting that premating isolation in cichlids is often fragile and context dependent. The observed lack of complete reproductive isolation is supported by past and present hybridization events that have contributed to diversity by creating novel allelic combinations. On the other hand, our meta-analysis highlights that intrinsic postzygotic isolation might accumulate faster than assumed. Mild forms of genetic incompatibilities, such as sex ratio distortion, can already be observed among closely related species. Therefore, cessation of gene flow by strong reproductive isolation in cichlids requires a combination of premating prezygotic isolation supplemented with intrinsic and extrinsic postzygotic barriers. Further, we suggest crucial next steps to improve our knowledge about reproductive barriers in cichlids to understand the evolutionary dynamics of pre- and postzygotic isolation mechanisms during adaptive radiations. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Lack of intrinsic postzygotic isolation in haplodiploid male hybrids despite high genetic distance

Evolutionary biologists have long been interested in understanding the mechanisms underlying Haldane’s rule. The explanatory theories of dominance and faster-X, which are based on recessive alleles being expressed in the heterogametic sex, have been proposed as common mechanisms. These mechanisms predict that greater hemizygosity leads to both faster evolution and greater expression of intrinsic postzygotic isolation. Under these mechanisms, haplodiploids should evolve and express intrinsic postzygotic isolation faster than diploids because the entire genome is analogous to a sex chromosome. Here, we measure sterility and inviability in hybrids between Neodiprion pinetum and N. lecontei, a pair of haplodiplopids that differ morphologically, behaviorally, and genetically. We compare the observed isolation to that expected from published estimates of isolation in diploids at comparable levels of genetic divergence. We find that both male and female hybrids are viable and fertile, which is less isolation than expected. We then discuss several potential explanations for this surprising lack of isolation, including alternative mechanisms for Haldane’s rule and a frequently overlooked quirk of haplodiploid genetics that may slow the emergence of complete intrinsic postzygotic isolation in hybrid males. Finally, we describe how haplodiploids, an underutilized resource, can be used to differentiate between mechanisms of Haldane’s rule.