Intrinsic Postzygotic Barriers Research Articles

The role of conflict in shaping plant biodiversity.

Although intrinsic postzygotic reproductive barriers can play a fundamental role in speciation, their underlying evolutionary causes are widely debated. One hypothesis is that incompatibilities result from genomic conflicts. Here, I synthesize the evidence that conflict generates incompatibilities in plants, thus playing a creative role in plant biodiversity. While much evidence supports a role for conflict in several classes of incompatibility, integrating knowledge of incompatibility alleles with natural history can provide further essential tests. Moreover, comparative work can shed light on the relative importance of conflict in causing incompatibilities, including the extent to which their evolution is repeatable. Together, these approaches can provide independent lines of evidence that conflict causes incompatibilities, cementing its role in plant speciation.

Do parapatric populations of the ticks Amblyomma tonelliae Nava, Beati & Labruna, 2014 and Amblyomma sculptum Berlese, 1888 (Acari: Ixodidae) hybridize?

This work aimed to determine if the tick species, Amblyomma sculptum and Amblyomma tonelliae, hybridize along their contact zones in Argentina. Free-living adults and nymphs of A. sculptum and A. tonelliae were collected in seven sampling locations of northern Argentina. In four of them, the two species occur in parapatry (possible hybrid zone) whereas in the other three sites, only one species is known to occur. A total of 65 A. sculptum and 65 A. tonelliae from both, allopatric and parapatric populations, were analysed. The nuclear (ITS2) and mitochondrial (COI and 12SrDNA) gene sequences of each tick were amplified and analysed to verify whether or not they could reveal the presence of hybrids among the parapatric samples. No morphological and molecular evidence was found to support the hypothesis of ongoing natural hybridization. Intrinsic postzygotic barriers may be the cause of lack of gene flow between the two species in areas of co-ocurrence. The results can be explained by the length of time the two lineages spent in allopatry since the middle of the Miocene and before their respective distribution range expanded again reaching a narrow secondary contact zone.

Three problems in the genetics of speciation by selection

Speciation is the process by which barriers to gene flow evolve between populations. Although we now know that speciation is largely driven by natural selection, knowledge of the agents of selection and the genetic and genomic mechanisms that facilitate divergence is required for a satisfactory theory of speciation. In this essay, we highlight three advances/problems in our understanding of speciation that have arisen from studies of the genes and genomic regions that underlie the evolution of reproductive isolation. First, we describe how the identification of “speciation” genes makes it possible to identify the agents of selection causing the evolution of reproductive isolation, while also noting that the link between the genetics of phenotypic divergence and intrinsic postzygotic reproductive barriers remains tenuous. Second, we discuss the important role of recombination suppressors in facilitating speciation with gene flow, but point out that the means and timing by which reproductive barriers become associated with recombination cold spots remains uncertain. Third, we establish the importance of ancient genetic variation in speciation, although we argue that the focus of speciation studies on evolutionarily young groups may bias conclusions in favor of ancient variation relative to new mutations.

Genomic introgression from a distant congener in the Levant fritillary butterfly, Melitaea acentria

Introgressive hybridization is more common in nature than previously thought, and its role and creative power in evolution is hotly discussed but not completely understood. Introgression occurs more frequently in sympatry between recently diverged taxa, or when the speciation process has not yet been completed. However, there are relatively few documented cases of hybridization that erodes reproductive barriers between distantly related species. Here, we use whole genome and mitochondrial data to examine how introgression from a distant congener affects pattern of genetic differentiation in the Levant fritillary butterfly Melitaea acentria. We show that this local taxon has evolved as a peripatric geographic isolate of the widespread Melitaea persea, and that there has been significant unidirectional gene flow from the sympatric, nonclosely related Melitaea didyma to M.acentria. We found direct evidence of ongoing sporadic hybridization between M.didyma and M.acentria, which are separated by at least 5million years of independent evolution. Elevated differentiation and lower level of introgression on the sex Z chromosome compared to autosomes suggest that the Z chromosome has accumulated loci acting as intrinsic postzygotic barriers. Our results show that introgression from M.didyma has been an additional source of nucleotide diversity in the M.acentria population, providing material for drift and selection.

Intrinsic postzygotic barriers constrain cross‐fertilisation between two hybridising sibling rotifer species of the Brachionus calyciflorus species complex

Abstract Brachionus calyciflorus is a recently described monogonont rotifer species complex that comprises four species. The observation of hybridisation between two of these species challenges this species delimitation. The mechanisms of reproductive isolation essential to the maintenance of species integrity remain unclear. Here, we conducted upscaled hybridisation experiments to obtain large numbers of hybrid and non‐hybrid dormant propagules. Through hatching assays, we compared the zygote viability of hybrid with non‐hybrid dormant propagules. Furthermore, we investigated populations of F1 hybrid clones and assessed their clonal growth rate and the ability to reproduce sexually. Our results demonstrated higher rates of morphological abnormality and associated mortality in dormant propagules of hybrids compared to non‐hybrids yet hatching rates of healthy‐looking propagules proved similar. F1 hybrids exhibited high clonal population growth rates, nevertheless, we also observed strong differences between clones and a strong influence of parental genotype identity. Two‐thirds of the F1 hybrid clones showed a low incidence of sexual reproduction and almost never produced dormant propagules. Clones with high population growth rates seemed to invest less in sexual reproduction. Our results clearly demonstrate the existence of intrinsic postzygotic barriers caused by relatively high mortality of dormant propagules. Furthermore, the low ability of most hybrid clones to engage in sexual reproduction may reduce the long‐term fitness of hybrid clones. These postzygotic barriers probably impede genetic exchange between parental species and contribute to the maintenance of their integrity.

Assessment of the ecologically dependent post-zygotic isolation between Anopheles coluzzii and Anopheles gambiae.

Within the Anopheles gambiae complex, the sibling species An. coluzzii and An. gambiae are undergoing sympatric speciation. These species are characterized by rare hybrids in most of their geographical distribution. A strong assortative mating mediated by spatial swarm segregation has been shown whereas no intrinsic post-zygotic barriers have been found in laboratory conditions. To test the role of the hybridisation in reproductive isolation in natural populations transplant experiment are therefore needed to establish the significance of post-zygotic barriers. Previous studies indicated that predation is one of the major forces driving ecological divergence between An. gambiae and An. coluzzii. Here we extended these studies to their hybrids. Parental species and their F1 hybrids from reciprocal crosses were generated by the forced-mating technique as follows: female An. coluzzii × male An. coluzzii; female An. coluzzii × male An. gambiae; female An. gambiae × male An. coluzzii and female An. gambiae × Male An. gambiae. First instar larvae of each group from the crossing (here after An. coluzzii, Hybrid COL/GAM, Hybrid GAM/COL and An. gambiae, respectively) were transplanted in a field experiment with predation effect. Emergence success, development time of larvae and body size of the newly emerging adults were estimated as fitness components and then compared between parental species and F1 hybrids in absence and in presence of predators. Our findings confirm that An. coluzzii had higher fitness than An. gambiae in presence of predators versus in absence of predators. Moreover, the fitness of the F1 hybrid COL/GAM whose female parent was An. coluzzii matched that of An. coluzzii while that of the F1 reciprocal hybrid GAM/COL was similar to An. gambiae.

The importance of intrinsic postzygotic barriers throughout the speciation process.

Intrinsic postzygotic barriers can play an important and multifaceted role in speciation, but their contribution is often thought to be reserved to the final stages of the speciation process. Here, we review how intrinsic postzygotic barriers can contribute to speciation, and how this role may change through time. We outline three major contributions of intrinsic postzygotic barriers to speciation. (i) reduction of gene flow: intrinsic postzygotic barriers can effectively reduce gene exchange between sympatric species pairs. We discuss the factors that influence how effective incompatibilities are in limiting gene flow. (ii) early onset of species boundaries via rapid evolution: intrinsic postzygotic barriers can evolve between recently diverged populations or incipient species, thereby influencing speciation relatively early in the process. We discuss why the early origination of incompatibilities is expected under some biological models, and detail how other (and often less obvious) incompatibilities may also serve as important barriers early on in speciation. (iii) reinforcement: intrinsic postzygotic barriers can promote the evolution of subsequent reproductive isolation through processes such as reinforcement, even between relatively recently diverged species pairs. We incorporate classic and recent empirical and theoretical work to explore these three facets of intrinsic postzygotic barriers, and provide our thoughts on recent challenges and areas in the field in which progress can be made. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Sexual isolation with and without ecological isolation in marine isopods Jaera albifrons and J.praehirsuta.

Sexual barriers associated with mate choice are often found to be associated with some level of ecological isolation between species. The independence and relative strength of sexual isolation are thus difficult to assess. Here, we take advantage of a pair of marine isopod species (Jaera albifrons and J.praehirsuta) that show sexual isolation and coexist in populations where they share the same microhabitat or not (i.e. without or with ecological isolation). We estimated the strength of sexual isolation between J.albifrons and J.praehirsuta using no-choice trials and a multiple-choice experimental population. We found that sexual isolation is strong in both the presence and the absence of ecological isolation, but that it is asymmetric and fails to prevent interspecific gene flow entirely. First-generation intrinsic post-zygotic barriers were low, and there was no sexual isolation within J.praehirsuta across habitats. The J.albifrons/J.praehirsuta species pair thus provides an example where the role of sexual isolation as a barrier to gene flow (a) does not depend upon current ecological isolation, (b) seems to have evolved independently of local ecological conditions, but (c) is insufficient to complete speciation entirely on its own.

Intraspecific genetic divergence within Helianthus niveus and the status of two new morphotypes from Mexico.

Collecting and characterizing the genetic diversity of wild relatives of crops can contribute importantly to sustainable crop production and food security. Wild sunflower, Helianthus niveus, occurs in arid regions in western North America and is partially cross-compatible with the cultivated sunflower (H. annuus). We assessed phylogenetic relationships and patterns of genetic divergence among three previously described subspecies (subsp. niveus, subsp. canescens, and subsp. tephrodes) as well as two new morphotypes of H. niveus recently discovered in extreme drought and dune habitats in Baja California, Mexico. We measured 50 plants growing in a common garden for 27 morphological traits and conducted principal component analysis to assess patterns of phenotypic variation. Genome size of each accession was determined using flow cytometry. Pollen viability of first generation hybrids between taxa was tested to infer the strength of intrinsic postzygotic reproductive barriers. Finally, genotyping-by-sequencing data were used to investigate the genetic structure and phylogenetic relationships among the previously described subspecies and new morphotypes. The intraspecific genetic and phenotypic divergence of H. niveus populations closely tracks their geographical distribution. Subspecies niveus is phenotypically, genetically, and reproductively distinct from the other two subspecies and has a larger genome. Therefore, H. niveus as currently circumscribed should be considered to contain two distinct species, H. niveus and H. tephrodes. ABBA-BABA tests revealed substantial introgression between subsp. canescens and its sympatric congener H. petiolaris, which might contribute to their morphological similarities. The two new morphotypes collected in Mexico represent local ecotypes of subsp. niveus that occur in extreme drought and dune environments. Mantel tests showed a strong positive correlation between genetic and geographic distances. We conclude that geographic isolation is primarily responsible for intraspecific genomic divergence within H. niveus, while patterns of phenotypic variation appear to have been shaped by ecological selection and interspecific introgression.

Reproductive isolation and the maintenance of species boundaries in two serpentine endemic Jewelflowers.

Speciation occurs when reproductive barriers substantially reduce gene flow between lineages. Understanding how specific barriers contribute to reproductive isolation offers insight into the initial forces driving divergence and the evolutionary and ecological processes responsible for maintaining diversity. Here, we quantified multiple pre- and post-pollination isolating barriers in a pair of closely related California Jewelflowers (Streptanthus, Brassicaceae) living in an area of sympatry. S. breweri and S. hesperidis are restricted to similar serpentine habitats; however, populations are spatially isolated at fine-scales and rarely co-occur in intermixed stands. Several intrinsic postzygotic barriers were among the strongest we quantified, yet, postzygotic barriers currently contribute little to overall reproductive isolation due to the cumulative strength of earlier-acting extrinsic barriers, including spatial isolation, and flowering time and pollinator differences. Data from multiple years suggest that pre-pollination barriers may have different strengths depending on annual environmental conditions. Similarly, crossing data suggest that the strength of intrinsic isolation may vary among different population pairs. Estimates of total reproductive isolation in S. breweri and S. hesperidis are robust to uncertainty and variability in individual barrier strength estimates, demonstrating how multiple barriers can act redundantly to prevent gene flow between close relatives living in sympatry.

Ecological divergence plays an important role in strong but complex reproductive isolation in campions (Silene).

New species arise through the evolution of reproductive barriers between formerly interbreeding lineages. Yet, comprehensive assessments of potential reproductive barriers, which are needed to make inferences on processes driving speciation, are only available for a limited number of systems. In this study, we estimated individual and cumulative strengths of seven prezygotic and six postzygotic reproductive barriers between the recently diverged taxa Silene dioica (L.) Clairv. and S. latifolia Poiret using both published and new data. A combination of multiple partial reproductive barriers resulted in near-complete reproductive isolation between S. dioica and S. latifolia, consistent with earlier estimates of gene flow between the taxa. Extrinsic barriers associated with adaptive ecological divergence were most important, while intrinsic postzygotic barriers had moderate individual strength but contributed only little to total reproductive isolation. These findings are in line with ecological divergence as driver of speciation. We further found extensive variation in extrinsic reproductive isolation, ranging from sites with very strong selection against migrants and hybrids to intermediate sites where substantial hybridization is possible. This situation may allow for, or even promote, heterogeneous genetic divergence.

Sexual imprinting and speciation between two Peromyscus species.

Sexual isolation, a reproductive barrier, can prevent interbreeding between diverging populations or species. Sexual isolation can have a clear genetic basis; however, it may also result from learned mate preferences that form via sexual imprinting. Here, we demonstrate that two sympatric species of mice-the white-footed mouse (Peromyscus leucopus) and its sister species, the cotton mouse (P. gossypinus)-hybridize only rarely in the wild despite co-occurrence in the same habitat and lack of any measurable intrinsic postzygotic barriers in laboratory crosses. We present evidence that strong conspecific mating preferences in each species result in significant sexual isolation. We find that these preferences are learned in at least one species: P. gossypinus sexually imprints on its parents, but in P. leucopus, additional factors influence mating preferences. Our study demonstrates that sexual imprinting contributes to reproductive isolation that reduces hybridization between otherwise interfertile species, supporting the role for learning in mammalian speciation.

Multiple strong postmating and intrinsic postzygotic reproductive barriers isolate florally diverse species of Jaltomata (Solanaceae).

Divergence in phenotypic traits often contributes to premating isolation between lineages, but could also promote isolation at postmating stages. Phenotypic differences could directly result in mechanical isolation or hybrids with maladapted traits; alternatively, when alleles controlling these trait differences pleiotropically affect other components of development, differentiation could indirectly produce genetic incompatibilities in hybrids. Here, we determined the strength of nine postmating and intrinsic postzygotic reproductive barriers among 10 species of Jaltomata (Solanaceae), including species with highly divergent floral traits. To evaluate the relative importance of floral trait diversification for the strength of these postmating barriers, we assessed their relationship to floral divergence, genetic distance, geographical context, and ecological differences, using conventional tests and a new linear-mixed modeling approach. Despite close evolutionary relationships, all species pairs showed moderate to strong isolation. Nonetheless, floral trait divergence was not a consistent predictor of the strength of isolation; instead this was best explained by genetic distance, although we found evidence for mechanical isolation in one species, and a positive relationship between floral trait divergence and fruit set isolation across species pairs. Overall, our data indicate that intrinsic postzygotic isolation is more strongly associated with genome-wide genetic differentiation, rather than floral divergence.

Components of reproductive isolation between the closely related grasshopper species Chorthippus biguttulus and C. mollis

The formation and maintenance of species in nature is accomplished by the evolution of reproductive isolating mechanisms. To understand patterns of speciation and coexistence between species, it is crucial to obtain a complete synopsis of reproductive isolating barriers. We identified multiple reproductive isolation barriers between two closely related species, Chorthippus biguttulus and Chorthippus mollis, and quantified their respective contributions to isolation. To this end, we produced hybrids and backcrosses in the laboratory to examine reproductive isolation at multiple stages in the life history. The prezygotic barriers, based on chemical and acoustic cues, are currently the strongest impediments to gene flow between C. biguttulus and C. mollis. This indicates an important role for sexual selection in the maintenance of species isolation. However, extrinsic and intrinsic postzygotic isolation barriers also contributed to reproductive isolation. The virtual sterility of F1 hybrid males was based on both the dysfunctionality of their testes and intermediate behavioral mating traits (behavioral sterility). This study demonstrates that a cascade of reproductive isolating mechanisms reduces the gene flow between C. biguttulus and C. mollis. Our results further demonstrate that the courtship display in these species consists of multimodal signals and indicates a key role of chemical cues in reproductive isolation and speciation in grasshoppers. The identification of species isolating mechanisms is essential for understanding the processes that drive speciation. A profound understanding of reproductive isolating mechanisms and their fitness consequences in a system is required to predict a specific speciation scenario. Members of the grasshopper subfamily Gomphocerinae show an enormous diversity and complexity in courtship behavior, especially in acoustic displays. Here, we demonstrate that non-acoustic and postzygotic isolation mechanisms also strongly contribute to reproductive isolation between the closely related grasshopper species, C. biguttulus and C. mollis. In addition, our results suggest that ongoing gene flow between this species pair is unlikely and that sexual selection plays an important role in the maintenance of species isolation.

Incipient ecological speciation between successional varieties of a dominant tree involves intrinsic postzygotic isolating barriers.

Whereas disruptive selection imposed by heterogeneous environments can lead to the evolution of extrinsic isolating barriers between diverging populations, the evolution of intrinsic postzygotic barriers through divergent selection is less certain. Long‐lived species such as trees may be especially slow to evolve intrinsic isolating barriers. We examined postpollination reproductive isolating barriers below the species boundary, in an ephemeral hybrid zone between two successional varieties of the landscape‐dominant Hawaiian tree, Metrosideros polymorpha, on volcanically active Hawai'i Island. These archipelago‐wide sympatric varieties show the weakest neutral genetic divergence of any taxon pair on Hawai'i Island but significant morphological and ecological differentiation consistent with adaptation to new and old lava flows. Cross‐fertility between varieties was high and included heterosis of F1 hybrids at the seed germination stage, consistent with a substantial genetic load apparent within varieties through low self‐fertility and a lack of self‐pollen discrimination. However, a partial, but significant, barrier was observed in the form of reduced female and male fertility of hybrids, especially backcross hybrids, consistent with the accumulation of genetic incompatibilities between varieties. These results suggest that partial intrinsic postzygotic barriers can arise through disruptive selection acting on large, hybridizing populations of a long‐lived species.

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.

On the persistence of reproductive barriers in Eucalyptus: the bridging of mechanical barriers to zygote formation by F1 hybrids is counteracted by intrinsic post-zygotic incompatibilities.

Many previous studies conclude that pre-zygotic barriers such as mechanical isolation account for most reproductive isolation between pairs of taxa. However, the inheritance and persistence of barriers such as these after the first generation of hybridization is rarely quantified, even though it is a vital consideration in understanding gene flow potential. There is an asymmetrical pre-zygotic mechanical barrier to hybridization between Eucalyptus nitens and Eucalyptus globulus, which completely prevents small-flowered E. nitens pollen from mating with large E. globulus flowers, while the reverse cross is possible. We aimed to determine the relative importance of pre- and post-zygotic barriers in preventing gene flow following secondary contact between E. nitens and E. globulus, including the inheritance of barriers in advanced-generation hybrids. Experimental crossing was used to produce outcrossed E. nitens, E. globulus and their F1, F2, BCg and BCn hybrids. The strength and inheritance of a suite of pre- and post-zygotic barriers were assessed, including 20-year survival, growth and reproductive capacity. The mechanical barrier to hybridization was lost or greatly reduced in the F1 hybrid. In contrast, intrinsic post-zygotic barriers were strong and persistent. Line-cross analysis indicated that the outbreeding depression in the hybrids was best explained by epistatic loss. The removal of strong mechanical barriers between E. nitens and E. globulus allows F1 hybrids to act as a bridge for bi-directional gene flow between these species. However, strong and persistent post-zygotic barriers exist, meaning that wherever F1 hybridization does occur, intrinsic post-zygotic barriers will be responsible for most reproductive isolation in this system. This potential transient nature of mechanical barriers to zygote formation due to additive inheritance in hybrids appears under-appreciated, and highlights the often important role that intrinsic post-mating barriers play in maintaining species boundaries at zones of secondary contact.

Does extreme asymmetric dominance promote hybridization between Anopheles coluzzii and Anopheles gambiae s.s. in seasonal malaria mosquito communities of West Africa?

BackgroundAnopheles gambiae s.s. and An. coluzzii are two of the most important malaria vector species in sub-Saharan Africa. These recently-diverged sibling species do not exhibit intrinsic post-zygotic barriers to reproduction and are thought to be separated by strong assortative mating combined with selection against hybrids. At present, little is known about the ecological conditions that determine hybridization and introgression between these cryptic taxa.MethodsSwarm segregation and assortative mating were studied in Western Burkina Faso in the villages of Vallée du Kou (VK7) and Soumousso which differed in terms of which sibling species was much rarer than the other, and in Bana where both occurred in similar proportions. Swarms and pairs in copula were collected and genotyped, the proportion of intra and interspecific mating determined, and interspecific sperm transfer checked genetically. Females were collected through larval and adult indoor collections and genotyped or sexed-and-genotyped via a novel multiplex PCR.ResultsA total of 3,687 males and 220 females were collected and genotyped from 109 swarms. Only 3 swarms were composed of males from both species, and these were from the village of VK7 where An. gambiae s.s. was comparatively rare. Mixed-species pairs captured in copula were only detected in that area and made for 3.62 % and 100 % of mating pairs involving An. coluzzii and An. gambiae s.s. individuals, respectively. The high An. gambiae s.s. cross-mating rate was mirrored by high rates of hybridizations estimated from female larvae and adults indoor collections. This contrasted with Soumousso, where despite being much less common than An. gambiae s.s., An. coluzzii males did not form mixed swarms, females were not found in interspecific swarms or copula and hybridization rates were low in both sibling species.ConclusionsThese data suggest that ecological conditions leading to rare An. gambiae s.s. in populations dominated by An. coluzzii may promote a breakdown of spatial swarm segregation and assortative mating between the two species. The lower overall hybridization rates observed at the larval and adult indoor stages compared to cross-mating rates support the idea that post-mating selection processes acting against hybrids may occur mostly prior to and/or at the early larval stages.

Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution.

Drosophila mauritiana is an Indian Ocean island endemic species that diverged from its two sister species, Drosophila simulans and Drosophila sechellia, approximately 240,000 years ago. Multiple forms of incomplete reproductive isolation have evolved among these species, including sexual, gametic, ecological, and intrinsic postzygotic barriers, with crosses among all three species conforming to Haldane’s rule: F1 hybrid males are sterile and F1 hybrid females are fertile. Extensive genetic resources and the fertility of hybrid females have made D. mauritiana, in particular, an important model for speciation genetics. Analyses between D. mauritiana and both of its siblings have shown that the X chromosome makes a disproportionate contribution to hybrid male sterility. But why the X plays a special role in the evolution of hybrid sterility in these, and other, species remains an unsolved problem. To complement functional genetic analyses, we have investigated the population genomics of D. mauritiana, giving special attention to differences between the X and the autosomes. We present a de novo genome assembly of D. mauritiana annotated with RNAseq data and a whole-genome analysis of polymorphism and divergence from ten individuals. Our analyses show that, relative to the autosomes, the X chromosome has reduced nucleotide diversity but elevated nucleotide divergence; an excess of recurrent adaptive evolution at its protein-coding genes; an excess of recent, strong selective sweeps; and a large excess of satellite DNA. Interestingly, one of two centimorgan-scale selective sweeps on the D. mauritiana X chromosome spans a region containing two sex-ratio meiotic drive elements and a high concentration of satellite DNA. Furthermore, genes with roles in reproduction and chromosome biology are enriched among genes that have histories of recurrent adaptive protein evolution. Together, these genome-wide analyses suggest that genetic conflict and frequent positive natural selection on the X chromosome have shaped the molecular evolutionary history of D. mauritiana, refining our understanding of the possible causes of the large X-effect in speciation.

Demographic Divergence History of Pied Flycatcher and Collared Flycatcher Inferred from Whole-Genome Re-sequencing Data

Profound knowledge of demographic history is a prerequisite for the understanding and inference of processes involved in the evolution of population differentiation and speciation. Together with new coalescent-based methods, the recent availability of genome-wide data enables investigation of differentiation and divergence processes at unprecedented depth. We combined two powerful approaches, full Approximate Bayesian Computation analysis (ABC) and pairwise sequentially Markovian coalescent modeling (PSMC), to reconstruct the demographic history of the split between two avian speciation model species, the pied flycatcher and collared flycatcher. Using whole-genome re-sequencing data from 20 individuals, we investigated 15 demographic models including different levels and patterns of gene flow, and changes in effective population size over time. ABC provided high support for recent (mode 0.3 my, range <0.7 my) species divergence, declines in effective population size of both species since their initial divergence, and unidirectional recent gene flow from pied flycatcher into collared flycatcher. The estimated divergence time and population size changes, supported by PSMC results, suggest that the ancestral species persisted through one of the glacial periods of middle Pleistocene and then split into two large populations that first increased in size before going through severe bottlenecks and expanding into their current ranges. Secondary contact appears to have been established after the last glacial maximum. The severity of the bottlenecks at the last glacial maximum is indicated by the discrepancy between current effective population sizes (20,000–80,000) and census sizes (5–50 million birds) of the two species. The recent divergence time challenges the supposition that avian speciation is a relatively slow process with extended times for intrinsic postzygotic reproductive barriers to evolve. Our study emphasizes the importance of using genome-wide data to unravel tangled demographic histories. Moreover, it constitutes one of the first examples of the inference of divergence history from genome-wide data in non-model species.