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The process of species formation is characterized by the accumulation of multiple reproductive barriers. The evolution of hybrid male sterility, or Haldane's rule, typically characterizes later stages of species formation, when reproductive isolation is strongest. Yet, understanding how quickly reproductive barriers evolve and their consequences for maintaining genetic boundaries between emerging species remains a challenging task because it requires studying taxa that hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus, where populations that show multiple reproductive barriers, including hybrid male sterility, hybridize in two natural hybrid zones. Using mitochondrial data, we infer that such populations diverged some 100,000 years ago, at the beginning of the last glacial cycle in Europe. Nuclear data show that contractions at multiple glacial refugia, and post‐glacial expansions have facilitated genetic differentiation between lineages that today interact in hybrid zones. We find extensive introgression throughout the sampled species range, irrespective of the current strength of reproductive isolation. Populations exhibiting hybrid male sterility in two hybrid zones show repeatable patterns of genomic differentiation, consistent with shared genomic constraints affecting ancestral divergence or with the role of those regions in reproductive isolation. Together, our results suggest that reproductive barriers that characterize late stages of species formation can evolve relatively quickly, particularly when associated with strong demographic changes. Moreover, we show that such barriers persist in the face of extensive gene flow, allowing future studies to identify associated genomic regions. [ABSTRACT FROM AUTHOR]

Hybrids between species are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex—a pattern known as Haldane's rule. The genetics of Haldane's rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary as a function of oocyte development. The Z chromosome has a major effect, similar to the 'large X effect' in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. By intersecting the list of genes within these QTLs with those differentially expressed in sterile and fertile hybrids, we identified three candidate genes with relevant phenotypes. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera and shows that it is produced by multiple complex epistatic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane's rule. [ABSTRACT FROM AUTHOR]

An introduction is presented on the theme of the periodical which is causes and consequences of the special connection between sex chromosomes and 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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

In two papers published at about the same time almost thirty years ago, Frank (Evolution, 45, 1991a, 262) and Hurst and Pomiankowski (Genetics, 128, 1991, 841) independently suggested that divergence of meiotic drive systems—comprising genes that cheat meiosis and genes that suppress this cheating—might provide a general explanation for Haldane's rule and the large X‐effect in interspecific hybrids. Although at the time, the idea was met with skepticism and a conspicuous absence of empirical support, the tide has since turned. Some of the clearest mechanistic explanations we have for hybrid male sterility involve meiotic drive systems, and several other cases of hybrid sterility are suggestive of a role for meiotic drive. In this article, I review these ideas and their descendants and catalog the current evidence for the meiotic drive model of speciation. In addition, I suggest that meiotic drive is not the only intragenomic conflict to involve the X chromosome and contribute to hybrid incompatibility. Sexually and parentally antagonistic selection pressures can also pit the X chromosome and autosomes against each other. The resulting intragenomic conflicts should lead to co‐evolution within populations and divergence between them, thus increasing the likelihood of incompatibilities in hybrids. I provide a sketch of these ideas and interpret some empirical patterns in the light of these additional X‐autosome conflicts. [ABSTRACT FROM AUTHOR]

Abstract: Hybrid sterility is a common first step in the evolution of postzygotic reproductive isolation. According to Haldane's Rule, it affects predominantly the heterogametic sex. While the genetic basis of hybrid male sterility in organisms with heterogametic males has been studied for decades, the genetic basis of hybrid female sterility in organisms with heterogametic females has received much less attention. We investigated the genetic basis of reproductive isolation in two closely related avian species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (L. luscinia), that hybridize in a secondary contact zone and produce viable hybrid progeny. In accordance with Haldane's Rule, hybrid females are sterile, while hybrid males are fertile, allowing gene flow to occur between the species. Using transcriptomic data from multiple individuals of both nightingale species, we identified genomic islands of high differentiation (FST) and of high divergence (Dxy), and we analysed gene content and patterns of molecular evolution within these islands. Interestingly, we found that these islands were enriched for genes related to female meiosis and metabolism. The islands of high differentiation and divergence were also characterized by higher levels of linkage disequilibrium than the rest of the genome in both species indicating that they might be situated in genomic regions of low recombination. This study provides one of the first insights into genetic basis of hybrid female sterility in organisms with heterogametic females. [ABSTRACT FROM AUTHOR]

The genetic structure and dynamics of hybrid zones provide crucial information for understanding the processes and mechanisms of evolutionary divergence and speciation. In general, higher levels of evolutionary divergence between taxa are more likely to be associated with reproductive isolation and may result in suppressed or strongly restricted hybridization. In this study, we examined two secondary contact zones between three deep evolutionary lineages in the common vole ( Microtus arvalis). Differences in divergence times between the lineages can shed light on different stages of reproductive isolation and thus provide information on the ongoing speciation process in M. arvalis. We examined more than 800 individuals for mitochondrial (mt DNA), Y-chromosome and autosomal markers and used assignment and cline analysis methods to characterize the extent and direction of gene flow in the contact zones. Introgression of both autosomal and mt DNA markers in a relatively broad area of admixture indicates selectively neutral hybridization between the least-divergent lineages ( Central and Eastern) without evidence for partial reproductive isolation. In contrast, a very narrow area of hybridization, shifts in marker clines and the quasi-absence of Y-chromosome introgression support a moving hybrid zone and unidirectional selection against male hybrids between the lineages with older divergence ( Central and Western). Data from a replicate transect further support non-neutral processes in this hybrid zone and also suggest a role for landscape history in the movement and shaping of geneflow profiles. [ABSTRACT FROM AUTHOR]

The susceptibility of the Y chromosome to sexual selection may make this chromosome an important player in the formation of reproductive isolating barriers, and ultimately speciation. Here, we investigate the role of the Y chromosome in phenotypic divergence and reproductive isolation of spinner dolphin ( Stenella longirostris) ecotypes. This species contains six known ecotypes (grouped into four subspecies) that exhibit striking differences in morphology, habitat and mating system, despite having adjacent or overlapping ranges and little genetic divergence at previously studied mt DNA and autosomal markers. We examined the phylogeographic structure for all six ecotypes across the species range ( n = 261, 17 geographic locations) using DNA sequences from three Y chromosome markers, two maternally inherited mitochondrial (mt DNA) markers, and a biparentally inherited autosomal intron. mt DNA and autosomal analyses revealed low divergence (most ΦST values <0.1) between ecotypes and geographic regions, concordant with previous studies. In contrast, Y intron analyses revealed fixed differences amongst the three most phenotypically divergent groups: S. l. longirostris vs. S. l. roseiventris vs. combined S. l. orientalis/ S. l. centroamericana/Tres Marias ecotypes). Another ecotype (whitebelly), previously postulated to be a hybrid between the two phenotypically most divergent ecotypes, had Y haplotypes from both putative parent ecotypes, supporting a hybrid designation. Reduced introgression of the Y chromosome has previously been observed in other organisms ranging from insects to terrestrial mammals, and here we demonstrate this phenomenon in a marine mammal with high dispersal capabilities. These results indicate that reduced introgression of the Y chromosome occurs in a wide taxonomic range of organisms and support the growing body of evidence that rapid evolution of the Y chromosome is important in evolutionary diversification. [ABSTRACT FROM AUTHOR]

Abstract Proportions of hybridization and introgression between the swallowtails Papilio hospiton , endemic to Sardinia and Corsica, and the holarctic Papilio machaon , were characterized using nine fully diagnostic and two differentiated allozyme loci and a mitochondrial DNA marker. Very low frequencies of F1 hybrids were detected in both Sardinia (0–4%, average 1.4%) and Corsica (0–3%, average 0.5%), as well as of first generation backcrosses (B1 ). No F2 were observed, in agreement with the hybrid breakdown detected in laboratory crosses. In spite of this minimal current gene exchange, specimens carrying introgressed alleles were found in high proportions in P. machaon but in lower proportions in P. hospiton . Introgression apparently occurred through past hybridization and repeated backcrossing, as evidenced by hybrid index scores and Bayesian assignment tests. Levels of introgression were low (0–1%) at two sex-linked loci and mitochondrial DNA, limited (0.4–2%) at three autosomal loci coding for dimeric enzymes, and high (up to 43%) at four autosomal loci coding for monomeric enzymes. Accordingly, selective filters are acting against foreign alleles, with differential effectiveness depending on the loci involved. The low levels of introgression at sex-linked loci and mitochondrial DNA are in agreement with Haldane's rule and suggest that introgression in P. machaon proceeds mainly through males, owing to a lower fitness of hybrid females. Papilio machaon populations showed higher levels of introgression in Sardinia than in Corsica. The role of reinforcement in the present reproductive isolation between P. machaon and P. hospiton is examined, as well as the evolutionary effects of introgressive hybridization between the two species. [ABSTRACT FROM AUTHOR]

Abstract Evolutionary history of Muscicapidae flycatchers is inferred from nuclear and mitochondrial DNA (mtDNA) sequence comparisons and population genetic analysis of nuclear and mtDNA markers. Phylogenetic reconstruction based on sequences from the two genomes yielded similar trees with respect to the order at which the species split off. However, the genetic distances fitted a nonlinear, polynomial model reflecting diminishing divergence rate of the mtDNA sequences compared to the nuclear DNA sequences. This could be explained by Haldane’s rule because genetic isolation might evolve more rapidly on the mitochondrial rather than the nuclear genome in birds. This is because hybrid sterility of the heterogametic sex (females) would predate that of the homogametic sex (males), leading to sex biased introgression of nuclear genes. Analyses of present hybrid zones of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) may indicate a slight sexual bias in rate of introgression, but the introgression rates were too low to allow proper statistical analyses. It is suggested, however, that the observed deviation from linearity can be explained by a more rapid mutational saturation of the mtDNA sequences than of the nuclear DNA sequences, as supported by analyses of third codon position transversions at two protein coding mtDNA genes. A phylogeographic scenario for the black and white flycatcher species is suggested based on interpretation of the genetic data obtained. Four species appear to have diverged from a common ancestor relatively simultaneously during the Pleistocene. After the last glaciation period, pied and collared flycatchers expanded their breeding ranges and eventually came into secondary contact in Central and Eastern Europe and on the Baltic Isles. [ABSTRACT FROM AUTHOR]

Abstract Hybridization may influence evolution in a variety of ways. If hybrids are less fit, the geographical range of ecologically divergent populations may be limited, and prezygotic reproductive isolation may be reinforced. If some hybrid genotypes are fitter than one or both parents, at least in some environments, then hybridization could make a positive contribution. Single alleles that are at an advantage in the alternative environment and genetic background will introgress readily, although such introgression may be hard to detect. ‘Hybrid speciation’, in which fit combinations of alleles are established, is more problematic; its likelihood depends on how divergent populations meet, and on the structure of epistasis. These issues are illustrated using Fisher’s model of stabilizing selection on multiple traits, under which reproductive isolation evolves as a side-effect of adaptation in allopatry. This confirms a priori arguments that while recombinant hybrids are less fit on average, some gene combinations may be fitter than the parents, even in the parental environment. Fisher’s model does predict heterosis in diploid F1s, asymmetric incompatibility in reciprocal backcrosses, and (when dominance is included) Haldane’s Rule. However, heterosis arises only when traits are additive, whereas the latter two patterns require dominance. Moreover, because adaptation is via substitutions of small effect, Fisher’s model does not generate the strong effects of single chromosome regions often observed in species crosses. [ABSTRACT FROM AUTHOR]