Intrinsic Post-zygotic Reproductive Isolation Research Articles

Bidirectional Introgression between Mus musculus domesticus and Mus spretus.

Introgressed variants from other species can be an important source of genetic variation because they may arise rapidly, can include multiple mutations on a single haplotype, and have often been pretested by selection in the species of origin. Although introgressed alleles are generally deleterious, several studies have reported introgression as the source of adaptive alleles—including the rodenticide-resistant variant of Vkorc1 that introgressed from Mus spretus into European populations of Mus musculus domesticus. Here, we conducted bidirectional genome scans to characterize introgressed regions into one wild population of M. spretus from Spain and three wild populations of M. m. domesticus from France, Germany, and Iran. Despite the fact that these species show considerable intrinsic postzygotic reproductive isolation, introgression was observed in all individuals, including in the M. musculus reference genome (GRCm38). Mus spretus individuals had a greater proportion of introgression compared with M. m. domesticus, and within M. m. domesticus, the proportion of introgression decreased with geographic distance from the area of sympatry. Introgression was observed on all autosomes for both species, but not on the X-chromosome in M. m. domesticus, consistent with known X-linked hybrid sterility and inviability genes that have been mapped to the M. spretus X-chromosome. Tract lengths were generally short with a few outliers of up to 2.7 Mb. Interestingly, the longest introgressed tracts were in olfactory receptor regions, and introgressed tracts were significantly enriched for olfactory receptor genes in both species, suggesting that introgression may be a source of functional novelty even between species with high barriers to gene flow.

Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution.

When gene regulatory networks diverge between species, their dysfunctional expression in inter-species hybrid individuals can create genetic incompatibilities that generate the developmental defects responsible for intrinsic post-zygotic reproductive isolation. Both cis- and trans-acting regulatory divergence can be hastened by directional selection through adaptation, sexual selection, and inter-sexual conflict, in addition to cryptic evolution under stabilizing selection. Dysfunctional sex-biased gene expression, in particular, may provide an important source of sexually-dimorphic genetic incompatibilities. Here, we characterize and compare male and female/hermaphrodite transcriptome profiles for sibling nematode species Caenorhabditis briggsae and C. nigoni, along with allele-specific expression in their F1 hybrids, to deconvolve features of expression divergence and regulatory dysfunction. Despite evidence of widespread stabilizing selection on gene expression, misexpression of sex-biased genes pervades F1 hybrids of both sexes. This finding implicates greater fragility of male genetic networks to produce dysfunctional organismal phenotypes. Spermatogenesis genes are especially prone to high divergence in both expression and coding sequences, consistent with a "faster male" model for Haldane's rule and elevated sterility of hybrid males. Moreover, underdominant expression pervades male-biased genes compared to female-biased and sex-neutral genes and an excess of cis-trans compensatory regulatory divergence for X-linked genes underscores a "large-X effect" for hybrid male expression dysfunction. Extensive regulatory divergence in sex determination pathway genes likely contributes to demasculinization of XX hybrids. The evolution of genetic incompatibilities due to regulatory versus coding sequence divergence, however, are expected to arise in an uncorrelated fashion. This study identifies important differences between the sexes in how regulatory networks diverge to contribute to sex-biases in how genetic incompatibilities manifest during the speciation process.

Speciation and the developmental alarm clock.

New species arise as the genomes of populations diverge. The developmental ‘alarm clock’ of speciation sounds off when sufficient divergence in genetic control of development leads hybrid individuals to infertility or inviability, the world awoken to the dawn of new species with intrinsic post-zygotic reproductive isolation. Some developmental stages will be more prone to hybrid dysfunction due to how molecular evolution interacts with the ontogenetic timing of gene expression. Considering the ontogeny of hybrid incompatibilities provides a profitable connection between ‘evo-devo’ and speciation genetics to better link macroevolutionary pattern, microevolutionary process, and molecular mechanisms. Here, we explore speciation alongside development, emphasizing their mutual dependence on genetic network features, fitness landscapes, and developmental system drift. We assess models for how ontogenetic timing of reproductive isolation can be predictable. Experiments and theory within this synthetic perspective can help identify new rules of speciation as well as rules in the molecular evolution of development.

Geographic contrasts between pre‐ and postzygotic barriers are consistent with reinforcement inHeliconiusbutterflies

Identifying the traits causing reproductive isolation and the order in which they evolve is fundamental to understanding speciation. Here, we quantify prezygotic and intrinsic postzygotic isolation among allopatric, parapatric, and sympatric populations of the butterflies Heliconius elevatus and Heliconius pardalinus. Sympatric populations from the Amazon (H. elevatus and H. p. butleri) exhibit strong prezygotic isolation and rarely mate in captivity; however, hybrids are fertile. Allopatric populations from the Amazon (H. p. butleri) and Andes (H. p. sergestus) mate freely when brought together in captivity, but the female F1 hybrids are sterile. Parapatric populations (H. elevatus and H. p. sergestus) exhibit both assortative mating and sterility of female F1s. Assortative mating in sympatric populations is consistent with reinforcement in the face of gene flow, where the driving force, selection against hybrids, is due to disruption of mimicry and other ecological traits rather than hybrid sterility. In contrast, the lack of assortative mating and hybrid sterility observed in allopatric populations suggests that geographic isolation enables the evolution of intrinsic postzygotic reproductive isolation. Our results show how the types of reproductive barriers that evolve between species may depend on geography.

Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group.

Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting different host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic effects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R. cingulata group.

Limited intrinsic postzygotic reproductive isolation despite chromosomal rearrangements between closely related sympatric species of small ermine moths (Lepidoptera: Yponomeutidae)

AbstractIn evolutionarily young species and sympatric host races of phytophagous insects, postzygotic incompatibility is often not yet fully developed, but reduced fitness of hybrids is thought to facilitate further divergence. However, empirical evidence supporting this hypothesis is limited. To assess the role of reduced hybrid fitness, we studied meiosis and fertility in hybrids of two closely related small ermine moths, Yponomeuta padella and Yponomeuta cagnagella, and determined the extent of intrinsic postzygotic reproductive isolation. We found extensive rearrangements between the karyotypes of the two species and irregularities in meiotic chromosome pairing in their hybrids. The fertility of reciprocal F1 and, surprisingly, also of backcrosses with both parental species was not significantly decreased compared with intraspecific offspring. The results indicate that intrinsic postzygotic reproductive isolation between these closely related species is limited. We conclude that the observed chromosomal rearrangements are probably not the result of an accumulation of postzygotic incompatibilities preventing hybridization. Alternative explanations, such as adaptation to new host plants, are discussed.

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.

The evolution of intrinsic reproductive isolation in the genus Cakile (Brassicaceae).

In theory, adaptive divergence can increase intrinsic post-zygotic reproductive isolation (RI), either directly via selection on loci associated with RI, or indirectly via linkage of incompatibility loci with loci under selection. To test this hypothesis, we measured RI at five intrinsic post-zygotic reproductive barriers between 18 taxa from the genera Cakile and Erucaria (Brassicaceae). Using a comparative framework, we tested whether the magnitude of RI was associated with genetic distance, geographic distance, ecological divergence and parental mating system. Early stages of post-zygotic RI related to F1 viability (i.e. initial seed set) tended to be stronger than later stages related to F1 fecundity (i.e. flower number, fruit number). Mating system significantly influenced early stages of RI, such that RI was lowest when the mother was selfing and father was outcrossing, consistent with an imbalance between sink strength and resistance to provisioning. We found little evidence that adaptive divergence accelerates the evolution of intrinsic post-zygotic RI, consistent with a nonecological model of evolution that predicts the nonlinear accumulation of RI and RI asymmetry with time (i.e. genetic distance), irrespective of adaptive divergence. Thus, although certain aspects of ecological divergence do not appear to have contributed strongly to the evolution of RI in this system, divergence in mating system actually reduced RI, suggesting that mating system evolution may play a significant role in speciation dynamics.

Negative epistasis: a route to intraspecific reproductive isolation in yeast?

Exploring the molecular bases of intraspecific reproductive isolation captures the ongoing phenotypic consequences of genetic divergence and provides insights into the early onset of speciation. Recent species-wide surveys using natural populations of yeasts demonstrated that intrinsic post-zygotic reproductive isolation segregates readily within the same species, and revealed the multiplicity of the genetic mechanisms underlying such processes. These advances deepened our current understandings and opened further perspectives regarding the complete picture of molecular and evolutionary origins driving the onset of intraspecific reproductive isolation in yeasts.

Genetics and Lineage-Specific Evolution of a Lethal Hybrid Incompatibility Between Drosophila mauritiana and Its Sibling Species

The Dobzhansky-Muller model posits that intrinsic postzygotic reproductive isolation--the sterility or lethality of species hybrids--results from the evolution of incompatible epistatic interactions between species: favorable or neutral alleles that become fixed in the genetic background of one species can cause sterility or lethality in the genetic background of another species. The kind of hybrid incompatibility that evolves between two species, however, depends on the particular evolutionary history of the causative substitutions. An allele that is functionally derived in one species can be incompatible with an allele that is functionally derived in the other species (a derived-derived hybrid incompatibility). But an allele that is functionally derived in one species can also be incompatible with an allele that has retained the ancestral state in the other species (a derived-ancestral hybrid incompatibility). The relative abundance of such derived-derived vs. derived-ancestral hybrid incompatibilities is unknown. Here, we characterize the genetics and evolutionary history of a lethal hybrid incompatibility between Drosophila mauritiana and its two sibling species, D. sechellia and D. simulans. We show that a hybrid lethality factor(s) in the pericentric heterochromatin of the D. mauritiana X chromosome, hybrid lethal on the X (hlx), is incompatible with a factor(s) in the same small autosomal region from both D. sechellia and D. simulans, Suppressor of hlx [Su(hlx)]. By combining genetic and phylogenetic information, we infer that hlx-Su(hlx) hybrid lethality is likely caused by a derived-ancestral incompatibility, a hypothesis that can be tested directly when the genes are identified.

Genetics of Speciation

The American Genetics Association (AGA) is a nonprofit membership society whose mission is to promote the study of genetics. To meet this obligation, the AGA publishes the Journal of Heredity and promotes research in all fields of genetics. The latter is accomplished through an annual meeting and symposium, as well as by sponsorship of special events, such as workshops and symposia in areas of interest to the AGA. In 2006, the annual meeting and symposium of the AGA was held from 21–24 July in Vancouver, British Columbia. The symposium, cosponsored with Molecular Ecology, was titled ‘‘Genetics of Speciation’’ and attracted close to 300 participants. Allen Orr was the recipient of the 2006 Wilhelmine Key Lectureship and gave the keynote lecture on ‘‘Speciation in Drosophila: from Phenotypes to Molecules.’’ Six articles from the symposium, which focus mostly on the genetics of postzygotic isolation, are published in this issue; another six more ecologically orientated papers will appear in Molecular Ecology. The lead article was authored by Allen Orr, J. P. Masly, and Nitin Phadnis, who review what we know about the genetics of intrinsic postzygotic reproductive isolation, at least with respect to genes underlying hybrid incompatibilities. Based on the 4 such genes that had been published by the symposium date (July 2006), Orr et al. note several striking patterns. In particular, most of these genes are evolving rapidly due to natural selection, a finding that supports the neo-Darwinian contention that reproductive isolation typically evolves as a by-product of adaptation. Given the seeming unity of these results, Orr et al. ask the provocative question ‘‘is the genetics of postzygotic isolation wrapped up?’’ That is, will more work in this area likely yield any truly novel results? Fortunately, new results discussed by Orr et al. suggest, in fact, that we are in for some real surprises. Most startling is the discovery that genetic conflict may frequently be the cause of rapid evolution of genes underlying intrinsic postzygotic barriers rather than adaptation to a new environment. Second, there is now evidence that microchromosomal rearrangements may sometimes be the cause of hybrid incompatibilities rather than the traditional Dobzhansky–Muller model. Another of the symposium speakers, Mohamed Noor, has been a leader in exploring nontraditional mechanisms for the evolution of intrinsic postzygotic barriers. In particular, he has developed and empirically tested a model in which genomic regions with low recombination (such as chromosomal inversions) allow Dobzhansky–Muller incompatibilities to accumulate despite ongoing gene flow. In this issue, Cirulli and Noor localize the break points of an inversion between two Drosophila species. Contrary to most other studies, there were no shared repetitive sequences between the 2 break point regions. Thus, the cause of the inversion remains a mystery. Most attempts to localize hybrid incompatibilities have employed experimental crosses, in which associations between molecular markers and sterility or inviability are used to identify chromosomal segments or genes that contribute to hybrid disorders. Although this approach has been highly successful, it is difficult to apply to nonmodel organisms, which can be challenging to rear in the laboratory or greenhouse. Thus, a number of authors have explored the possibility of using patterns of introgression in natural hybrid zones to localize genes or chromosomal rearrangements that contribute to isolation. In ‘‘Searching the Genomes of Inbred Mouse Strains for Incompatibilities that Reproductively Isolate Their Wild Relatives,’’ Payseur and Place successfully employ this strategy to identify pairs of loci that may contribute to reproductive isolation between 2 mice species. One of the early conclusions (above) from studies of the genes causing hybrid incompatibilities is that postzygotic isolation often appears to be a by-product of adaptation. Thus, Leonie Moyle asks whether quantitative trait loci (QTLs) underlying putative prezygotic isolating traits in tomatoes, which presumably have been shaped by natural selection, colocalize with QTLs for hybrid sterility. Unfortunately, there is little evidence for a causal association between prezygotic and postzygotic isolation. Intrinsic postzygotic isolation may also arise through genome doubling or polyploidy. However, polyploidy has other genetic and phenotypic consequences beyond reproductive isolation. One of themost interesting of these (and potentially most important) is the observation that large shifts in gene expression may accompany polyploidization. Because polyploidy may involve both interspecific hybridization and genome doubling, the effects of these two processes on gene expression often are confounded. In ‘‘Evolution of Duplicate Gene Expression in Polyploid and Hybrid Plants,’’ Journal of Heredity doi:10.1093/jhered/esl066 a The American Genetic Association. 2007. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org.

The origin of species

The origin of species