Asymmetric Introgression Research Articles

A consequential one-night stand: Episodic historical hybridization leads to mitochondrial takeover in sympatric desert ant-eating spiders

Disentangling the genomic intricacies underlying speciation and the causes of discordance between sources of evidence can offer remarkable insights into evolutionary dynamics. The ant-eating spider Zodarion nitidum, found across the Middle East and Egypt, displays yellowish and blackish morphs that co-occur sympatrically. These morphs additionally differ in behavioral and physiological features and show complete pre-mating reproductive isolation. In contrast, they possess similar sexual features and lack distinct differences in their mitochondrial DNA. We analyzed both Z. nitidum morphs and outgroups using genome-wide and additional mitochondrial DNA data. The genomic evidence indicated that Yellow and Black are reciprocally independent lineages without signs of recent admixture. Interestingly, the sister group of Yellow is not Black but Z. luctuosum, a morphologically distinct species. Genomic gene flow analyses pinpointed an asymmetric nuclear introgression event, with Yellow contributing nearly 5 % of its genome to Black roughly 320,000 years ago, intriguingly aligning with the independently estimated origin of the mitochondrial DNA of Black. We conclude that the blackish and yellowish morphs of Z. nitidum are long-diverged distinct species, and that the ancient and modest genomic introgression event registered resulted in a complete mitochondrial takeover of Black by Yellow. This investigation underscores the profound long-term effects that even modest hybridization events can have on the genome of organisms. It also exemplifies the utility of phylogenetic networks for estimating historical events and how integrating independent lines of evidence can increase the reliability of such estimations.

Structure of the hybrid zone between allied species of the common vole, Microtus arvalis and M. obscurus: Influence of genetic factors and landscape-geographic conditions

Patterns of introgression of several genetic markers across the hybrid zone between allied species of the common vole Microtus arvalis s. str. и M. obscurus were studied in four its sections: in northwest Nizhny Novgorod region, east Vladimir and southwest of Nizhny Novgorod regions, south Lipetsk region, and northwest Voronezh region. Analysis of the clinal variability for three molecular-genetic markers (cytb, tp53, SMCY11) and for karyotypes showed a structural similarity between the “Vladimir – Nizhny Novgorod”, “Nizhny Novgorod”, and “Voronezh” sections. The maximal width was shown for the cytb cline, the minimal width – for the SMCY11 cline; the tp53 cline and chromosomal cline occupy intermediate position for this parameter. Furthermore, in these transects the centre of the cline for the cytb is shifted southeastward (into the distribution range of M. obscurus) from the centres of three other clines. The revealed asymmetric introgression of mitochondrial genome from M. arvalis to M. obscurus may be explained by the fact that the hybrid zone was formed as a result of invasion of M. obscurus into the range of M. arvalis. The “Lipetsk” transect differs from three above-mentioned transects by very narrow clines with nearly coinciding centres. Such characteristics of the “Lipetsk” transect are obviously caused by localization of the hybrid zone in this section along river Voronezh. The obtained results led us to suppose that the structure of the studied hybrid zone is determined mainly by coinciding (or non-coinciding) of its centre with local physical barriers.

Recent secondary contact, genome-wide admixture, and asymmetric introgression of neo-sex chromosomes between two Pacific island bird species.

Secondary contact between closely related taxa represents a "moment of truth" for speciation-an opportunity to test the efficacy of reproductive isolation that evolved in allopatry and to identify the genetic, behavioral, and/or ecological barriers that separate species in sympatry. Sex chromosomes are known to rapidly accumulate differences between species, an effect that may be exacerbated for neo-sex chromosomes that are transitioning from autosomal to sex-specific inheritance. Here we report that, in the Solomon Islands, two closely related bird species in the honeyeater family-Myzomela cardinalis and Myzomela tristrami-carry neo-sex chromosomes and have come into recent secondary contact after ~1.1 my of geographic isolation. Hybrids of the two species were first observed in sympatry ~100 years ago. To determine the genetic consequences of hybridization, we use population genomic analyses of individuals sampled in allopatry and in sympatry to characterize gene flow in the contact zone. Using genome-wide estimates of diversity, differentiation, and divergence, we find that the degree and direction of introgression varies dramatically across the genome. For sympatric birds, autosomal introgression is bidirectional, with phenotypic hybrids and phenotypic parentals of both species showing admixed ancestry. In other regions of the genome, however, the story is different. While introgression on the Z/neo-Z-linked sequence is limited, introgression of W/neo-W regions and mitochondrial sequence (mtDNA) is highly asymmetric, moving only from the invading M. cardinalis to the resident M. tristrami. The recent hybridization between these species has thus enabled gene flow in some genomic regions but the interaction of admixture, asymmetric mate choice, and/or natural selection has led to the variation in the amount and direction of gene flow at sex-linked regions of the genome.

Digest: Asymmetrical introgression of belly coloration across a manakin hybrid zone in Panama.

How does sexual selection impact introgression dynamics across a hybrid zone? Long et al. (2024) used historical (1989-1994) and contemporary (2017-2020) samples to quantify the stability of a Panamanian hybrid zone between golden-collared manakins (Manacus vitellinus) and white-collared manakins (M. candei). Their analyses revealed a spatially stable hybrid zone, except for one trait, belly plumage coloration, which has introgressed into the distribution of the white-collared manakin. This finding suggests possible sexual selection for this trait.

Asymmetric Introgression and Cryptic Natural Hybridization between Two Species of Teucrium Section Polium (Lamiaceae) on the Balkan Peninsula.

In this work, we analyzed the morphology and genetic structure of Teucrium montanum, T. capitatum and their hybrid T. × rohlenae from three syntopic populations. A morphometric study showed that the parents and their hybrids exhibited continuous morphological variation, with the hybrid positioned exactly between the parents. Genetic analysis revealed that plants morphologically identified as T. × rohlenae are fertile hybrids that produce hybrid swarms dominated by later-generation hybrids. This suggests that introgression, rather than speciation, is the more likely outcome of hybridization between these plant species. The extent and direction of gene flow between the two species differed markedly between the three syntopic localities. At the Trilj locality, it was clearly unidirectional, with T. capitatum playing the dominant role. At the Sićevo locality, gene flow was slightly asymmetric, favoring the genetic background of T. capitatum, while at the Sliven site, it was completely asymmetric in the opposite direction. The extreme case of unidirectional gene flow was observed at the Trilj locality where plants morphologically identified as T. montanum could not be genetically distinguished from T. capitatum. This suggests that interspecific hybridization occurred long ago, leading to introgression and cryptic hybrids, blurring of species boundaries and generating evolutionary noise.

Interspecific Sharing of Closely Related Chloroplast Genome Haplotypes among Sclerophyllous Oaks in the Hot-Dry Valley of the Jinsha River, Southwestern China

Evergreen sclerophyllous oak forests (ESOFs) in southwestern China are a special vegetation type developed in response to the expansion of arid habitats after the uplift of the Himalayas. Here, we used chloroplast (cp) DNA and nuclear ribosomal (nr) DNA to investigate the fine-scale genetic variation patterns of six sympatric oaks (Quercus, Fagaceae) in the hot-dry valley ESOFs of the Jinsha River, southwestern China. Three cp genomes were assembled for each species. Nine cp genome haplotypes and 16 nrDNA haplotypes were identified based on single-nucleotide variants and indels. Our results demonstrated that discordance existed between the cpDNA and nrDNA phylogenies of the sclerophyllous oaks in section Ilex. The nrDNA phylogeny was consistent with species boundaries, while the cpDNA phylogeny was decoupled from taxonomy. Interspecific sharing of closely related cp genome haplotypes was detected between Quercus cocciferoides and the other two sclerophyllous oaks, Q. longispica and Q. franchetii. Specifically, Q. cocciferoides and Q. longispica sampled in a mixed stand exhibited two haplotypes that differed by a 9 bp indel. The local distribution of the two highly similar haplotypes suggested that they may have arisen from ancient introgression. Given that the two species have diverged for a long time, it is possible that the ancestral cp genome of one species was captured by another species through asymmetric introgression in early times, and an indel event occurred subsequently. Phylogenetic analyses using more previously published cp genome sequences indicated that Q. cocciferoides and Q. franchetii shared multiple cpDNA lineages of Ilex oaks, which may be caused by shared ancestral polymorphism and/or ancient introgression. Our study showed that at least three highly variable regions (ψycf1, ndhF-rpl32, and trnKUUU-rps16 or rpl32-trnLUAG) can distinguish the nine haplotypes identified by whole-cp genome sequences. These markers are useful for the evolutionary studies of the maternal lineages of oaks in hot-dry valley ESOFs.

Patterns of admixture and introgression in a mosaic Mytilus galloprovincialis and Mytilus edulis hybrid zone in SW England.

The study of hybrid zones offers important insights into speciation. Earlier studies on hybrid populations of the marine mussel species Mytilus edulis and Mytilus galloprovincialis in SW England provided evidence of admixture but were constrained by the limited number of molecular markers available. We use 57 ancestry-informative SNPs, most of which have been mapped genetically, to provide evidence of distinctive differences between admixed populations in SW England and asymmetrical introgression from M. edulis to M. galloprovincialis. We combine the genetic study with analysis of phenotypic traits of potential ecological and adaptive significance. We demonstrate that hybrid individuals have brown mantle edges unlike the white or purple in the parental species, suggesting allelic or non-allelic genomic interactions. We report differences in gonad development stage between the species consistent with a prezygotic barrier between the species. By incorporating results from publications dating back to 1980, we confirm the long-term stability of the hybrid zone despite higher viability of M. galloprovincialis. This stability coincides with a dramatic change in temperature of UK coastal waters and suggests that these hybrid populations might be resisting the effects of global warming. However, a single SNP locus associated with the Notch transmembrane signalling protein shows a markedly different pattern of variation to the others and might be associated with adaptation of M. galloprovincialis to colder northern temperatures.

The Case for a Nuclear Barcode: Using the CAD CPS Region for Species and Genus Level Discrimination in Beetles

DNA barcoding has revolutionized how we discover, identify, and detect species. A substantial foundation has been established with millions of mitochondrial cytochrome c oxidase I sequences freely available for eukaryotes. However, issues with COI ranging from uniparental inheritance and small genetic population sizes to nuclear and asymmetric introgression can impede its use. We propose using CAD as the “nuclear barcode” to complement the COI barcode and ameliorate these concerns. We focused on beetles from taxonomically diverse species-level studies that used COI and CAD. An ambiguous barcode gap was present between intra- and interspecific genetic distances in CAD and COI; this led to difficulty with automated gap detection methods. We found pseudogenes, problematic population structure, introgression, and incomplete lineage sorting represented in the COI data. A CAD gene tree illuminated these cryptic problems. Placement tests of species and outgroups using distance-based tree building were largely successful for CAD, demonstrating its phylogenetic signal at the species and genus levels. Species placement issues were typically unique to one locus, allowing for recognition of misdiagnosis. We conclude that a CAD barcode is a valuable tool for beetle diagnostics, metabarcoding, and faunistic surveys.

Detecting introgressive hybridization to maintain genetic integrity in endangered large waterbird: a case study in milky stork

Hybridization between milky stork (Mycteria cinerea) and painted stork (M. leucocephala) occurs frequently in captivity. Dusit Zoo is a captive breeding facility where storks with phenotypically ambiguous patterns have recently been observed, and their status remaining inconclusive. Here, we used a combination of phenotypic characters and genetic markers (cytochrome b and 14 microsatellite markers) to distinguish and identify hybrids from the two parental species (n = 114). Haplotype analysis revealed asymmetric mtDNA introgression from M. cinerea to M. leucocephala, with twelve morphologically classified M. leucocephala individuals carrying heterospecific mtDNA. Comprehensive biparental genetic assessments identified 33% of all three genetic clusters as admixed individuals, of which most were either F2 hybrids, backcrosses with M. leucocephala, or hybrids of unknown generation, implying weak premating isolation with the absence of intrinsic postzygotic isolation between parentals. Morphological analysis demonstrated that the absence or indistinctness of a black bar across the breast is the most noticeable trait to identify these hybrids. The endangered M. cinerea was found to have genomic contamination from M. leucocephala and vice versa, with at least 41 hybrid individuals being identified. These findings provide critical information for detecting hybrids and identifying suitable breeding stocks with genetic purity for future reintroduction and conservation management.

Translocation precipitates natural hybridisation and pervasive introgression between marine gastropods with divergent developmental modes

Assisted colonisation, the introduction of species beyond their historical range, is increasingly necessary for conserving species. However, empirical evidence of the long-term genetic outcomes of assisted colonisation is grossly lacking. A risk associated with moving species beyond their native range is the possibility of interspecific hybridisation with a closely related species, potentially resulting in outbreeding depression or the genetic swamping of a parental species. Here, we use a combination of genome-wide Single Nucleotide Polymorphism (SNP) markers and mitochondrial DNA sequencing to determine the long-term genetic consequences of introducing the intertidal periwinkle Bembicium vittatum (a direct developer) beyond its native range and into the native range of its congener Bembicium auratum (a species with planktotrophic larval dispersal). We found novel evidence of natural, multigenerational hybridisation between marine invertebrates with different modes of development. Intriguingly, introgression was highly asymmetrical initially, but became more evenly bidirectional as the population became more admixed. There was a significant decline in the frequency of alleles from the introduced B. vittatum over time, providing evidence of genetic swamping. The present study also provides potential evidence of outbreeding depression, in the form of cytonuclear incompatibilities, leading to the observed pattern of asymmetrical introgression. This study reveals the potential for unexpected mixing between species when reproductive barriers are not well understood, resulting in failure of pure B. vittatum to persist at the translocation site, a major concern associated with assisted colonisation. Without long-term genetic monitoring interspecific hybridisation between B. vittatum and B. auratum would have gone undetected, highlighting the importance of long-term monitoring to detect unintentional negative consequences of conservation translocations. Successful assisted colonisation requires an understanding of the potential for interspecific hybridisation between the threatened species and closely related native species, to reduce the risk of adverse outcomes.

Population structure and genome-wide evolutionary signatures reveal putative climate-driven habitat change and local adaptation in the large yellow croaker

The large yellow croaker (Larimichthyscrocea) is one of the most economically valuable marine fish in China and is a notable species in ecological studies owing to a serious collapse of wild germplasm in the past few decades. The stock division and species distribution, which have important implications for ecological protection, germplasm recovery, and fishery resource management, have been debated since the 1960s. However, it is still uncertain even how many stocks exist in this species. To address this, we evaluated the fine-scale genetic structure of large yellow croaker populations distributed along the eastern and southern Chinese coastline based on 7.64 million SNP markers. Compared with the widely accepted stock boundaries proposed in the 1960s, our results revealed that a climate-driven habitat change probably occurred between the Naozhou (Nanhai) Stock and the Ming-Yuedong (Mindong) Stock. The boundary between these two stocks might have shifted northwards from the Pearl River Estuary to the northern area of the Taiwan Strait, accompanied by highly asymmetric introgression. In addition, we found divergent landscapes of natural selection between the stocks inhabiting northern and southern areas. The northern population exhibited highly agminated signatures of strong natural selection in genes related to developmental processes, whereas moderate and interspersed selective signatures were detected in many immune-related genes in the southern populations. These findings establish the stock status and genome-wide evolutionary landscapes of large yellow croaker, providing a basis for conservation, fisheries management and further evolutionary biology studies.

Phylogeography and introgression between Pinus kesiya and Pinus yunnanensis in Southeast Asia

AbstractSoutheast Asia (SEA) has seen strong climatic oscillations and fluctuations in sea levels during the Quaternary. The impact of past climate changes on the evolution and distribution of local flora in SEA is still poorly understood. Here we aim to infer how the Quaternary climate change affects the evolutionary process and range shifts in two pine species. We investigated the population genetic structure and diversity using cytoplasmic DNA markers, and performed ecological niche modeling to reconstruct the species past distribution and to project range shift under future climates. We found substantial gene flow across the continuous distribution of the subtropical Pinus yunnanensis. In contrast, the tropical Pinus kesiya showed a strong population structure in accordance with its disjunct distribution across montane islands in Indochina and the Philippines. A broad hybrid zone of the two species occurs in southern Yunnan. Asymmetric introgression from the two species was detected in this zone with dominant mitochondrial gene flow from P. yunnanensis and chloroplast gene flow from P. kesiya. The observed population structure suggests a typical postglaciation expansion in P. yunnanensis, and a glacial expansion and interglacial contraction in P. kesiya. Ecological niche modeling supports the inferred demographic history and predicts a decrease in range size for P. kesiya under future climates. Our results suggest that tropical pine species in SEA have undergone evolutionary trajectories different from high latitude species related to their Quaternary climate histories. We also illustrate the need for urgent conservation actions in this fragmented landscape.

Comparison of plastid genomes and ITS of two sister species in Gentiana and a discussion on potential threats for the endangered species from hybridization

BackgroundGentiana rigescens Franchet is an endangered medicinal herb from the family Gentianaceae with medicinal values. Gentiana cephalantha Franchet is a sister species to G. rigescens possessing similar morphology and wider distribution. To explore the phylogeny of the two species and reveal potential hybridization, we adopted next-generation sequencing technology to acquire their complete chloroplast genomes from sympatric and allopatric distributions, as along with Sanger sequencing to produce the nrDNA ITS sequences.ResultsThe plastid genomes were highly similar between G. rigescens and G. cephalantha. The lengths of the genomes ranged from 146,795 to 147,001 bp in G. rigescens and from 146,856 to 147,016 bp in G. cephalantha. All genomes consisted of 116 genes, including 78 protein-coding genes, 30 tRNA genes, four rRNA genes and four pseudogenes. The total length of the ITS sequence was 626 bp, including six informative sites. Heterozygotes occurred intensively in individuals from sympatric distribution. Phylogenetic analysis was performed based on chloroplast genomes, coding sequences (CDS), hypervariable sequences (HVR), and nrDNA ITS. Analysis based on all the datasets showed that G. rigescens and G. cephalantha formed a monophyly. The two species were well separated in phylogenetic trees using ITS, except for potential hybrids, but were mixed based on plastid genomes. This study supports that G. rigescens and G. cephalantha are closely related, but independent species. However, hybridization was confirmed to occur frequently between G. rigescens and G. cephalantha in sympatric distribution owing to the lack of stable reproductive barriers. Asymmetric introgression, along with hybridization and backcrossing, may probably lead to genetic swamping and even extinction of G. rigescens.ConclusionG. rigescens and G. cephalantha are recently diverged species which might not have undergone stable post-zygotic isolation. Though plastid genome shows obvious advantage in exploring phylogenetic relationships of some complicated genera, the intrinsic phylogeny was not revealed because of matrilineal inheritance here; nuclear genomes or regions are hence crucial for uncovering the truth. As an endangered species, G. rigescens faces serious threats from both natural hybridization and human activities; therefore, a balance between conservation and utilization of the species is extremely critical in formulating conservation strategies.

Tandem Repeat DNA Provides Many Cytological Markers for Hybrid Zone Analysis in Two Subspecies of the Grasshopper Chorthippus parallelus.

Recent advances in next generation sequencing (NGS) have greatly increased our understanding of non-coding tandem repeat (TR) DNA. Here we show how TR DNA can be useful for the study of hybrid zones (HZ), as it serves as a marker to identify introgression in areas where two biological entities come in contact. We used Illumina libraries to analyse two subspecies of the grasshopper Chorthippus parallelus, which currently form a HZ in the Pyrenees. We retrieved a total of 152 TR sequences, and used fluorescent in situ hybridization (FISH) to map 77 families in purebred individuals from both subspecies. Our analysis revealed 50 TR families that could serve as markers for analysis of this HZ, using FISH. Differential TR bands were unevenly distributed between chromosomes and subspecies. Some of these TR families yielded FISH bands in only one of the subspecies, suggesting the amplification of these TR families after the geographic separation of the subspecies in the Pleistocene. Our cytological analysis of two TR markers along a transect of the Pyrenean hybrid zone showed asymmetrical introgression of one subspecies into the other, consistent with previous findings using other markers. These results demonstrate the reliability of TR-band markers for hybrid zone studies.

Asymmetrical lineage introgression and recombination in populations of Aspergillus flavus: Implications for biological control.

Aspergillus flavus is an agriculturally important fungus that causes ear rot of maize and produces aflatoxins, of which B1 is the most carcinogenic naturally-produced compound. In the US, the management of aflatoxins includes the deployment of biological control agents that comprise two nonaflatoxigenic A. flavus strains, either Afla-Guard (member of lineage IB) or AF36 (lineage IC). We used genotyping-by-sequencing to examine the influence of both biocontrol agents on native populations of A. flavus in cornfields in Texas, North Carolina, Arkansas, and Indiana. This study examined up to 27,529 single-nucleotide polymorphisms (SNPs) in a total of 815 A. flavus isolates, and 353 genome-wide haplotypes sampled before biocontrol application, three months after biocontrol application, and up to three years after initial application. Here, we report that the two distinct A. flavus evolutionary lineages IB and IC differ significantly in their frequency distributions across states. We provide evidence of increased unidirectional gene flow from lineage IB into IC, inferred to be due to the applied Afla-Guard biocontrol strain. Genetic exchange and recombination of biocontrol strains with native strains was detected in as little as three months after biocontrol application and up to one and three years later. There was limited inter-lineage migration in the untreated fields. These findings suggest that biocontrol products that include strains from lineage IB offer the greatest potential for sustained reductions in aflatoxin levels over several years. This knowledge has important implications for developing new biocontrol strategies.

Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): integrating data on nuclear and mitochondrial markers, vocalizations, and field observations

Zones of secondary contact provide a good opportunity to investigate the origin and dynamics of reproductive isolation between related populations. We analyzed genetic and phenotypic patterns and gene flow between two subspecies of the Eurasian magpie Pica pica s.l. which recently came into contact after presumably long periods of isolation. We describe the distribution of subspecies in a young contact zone at Argun’ river basin in southern Siberia where populations occur in parapatry and an older hybrid population in eastern Mongolia. Based on genome-wide SNP data, we analyzed patterns and strength of gene flow between the subspecies. Our results indicate occasional hybridization with backcrossing and asymmetric introgression along a wide range in Transbaikalia and locally in eastern Mongolia. Males of P. p. jankowskii apparently exhibit higher dispersal ability towards the west compared to P. p. leucoptera (towards the east). The former occasionally migrates to eastern Mongolia and Transbaikalia where introgression of nuclear, but not mitochondrial DNA was evident. Bioacoustic investigations showed differences between the subspecies in speed and structure of vocalization. We discovered intermediate calls of hybrid magpies and bilingual birds alternating calls that are typical for the two taxa. Furthermore, we found dramatically decreased reproductive success in hybridogeneous populations. By complementing our results with established phylogeographic patterns of P. pica s.l. based on a mitochondrial marker sequence, and considering indications of sterility of hybrids in the contact zone, we propose to elevate the two corresponding subspecies to species level: P. pica for the western form and P. serica for the eastern form.

Population-genomic analyses reveal bottlenecks and asymmetric introgression from Persian into iron walnut during domestication

BackgroundPersian walnut, Juglans regia, occurs naturally from Greece to western China, while its closest relative, the iron walnut, Juglans sigillata, is endemic in southwest China; both species are cultivated for their nuts and wood. Here, we infer their demographic histories and the time and direction of possible hybridization and introgression between them.ResultsWe use whole-genome resequencing data, different population-genetic approaches (PSMC and GONE), and isolation-with-migration models (IMa3) on individuals from Europe, Iran, Kazakhstan, Pakistan, and China. IMa3 analyses indicate that the two species diverged from each other by 0.85 million years ago, with unidirectional gene flow from eastern J. regia and its ancestor into J. sigillata, including the shell-thickness gene. Within J. regia, a western group, located from Europe to Iran, and an eastern group with individuals from northern China, experienced dramatically declining population sizes about 80 generations ago (roughly 2400 to 4000 years), followed by an expansion at about 40 generations, while J. sigillata had a constant population size from about 100 to 20 generations ago, followed by a rapid decline.ConclusionsBoth J. regia and J. sigillata appear to have suffered sudden population declines during their domestication, suggesting that the bottleneck scenario of plant domestication may well apply in at least some perennial crop species. Introgression from introduced J. regia appears to have played a role in the domestication of J. sigillata.

DNA Identification and Diversity of the Vector Mosquitoes Culex pipiens s.s. and Culex torrentium in Belgium (Diptera: Culicidae)

This survey reports on the DNA identification and occurrence of Culex torrentium and Cx. pipiens s.s. in Belgium. These native disease-vector mosquito species are morphologically difficult to separate, and the biotypes of Cx. pipiens s.s. are morphologically indistinguishable. Culex torrentium and Cx. pipiens s.s. were identified using the COI and ACE2 loci. We recorded 1248 Cx. pipiens s.s. and 401 Cx. torrentium specimens from 24 locations in Belgium (collected between 2017 and 2019). Culex pipiens biotypes pipiens and molestus, and their hybrids, were differentiated using fragment-size analysis of the CQ11 locus (956 pipiens and 227 molestus biotype specimens, 29 hybrids). Hybrids were observed at 13 out of 16 sympatric sites. These results confirm that both species are widespread in Belgium, but while Cx. torrentium revealed many COI haplotypes, Cx. pipiens s.s. showed only one abundant haplotype. This latter observation may either reflect a recent population-wide demographic or range expansion, or a recent bottleneck, possibly linked to a Wolbachia infection. Finally, new evidence is provided for the asymmetric but limited introgression of the molestus biotype into the pipiens biotype.

Neo-sex chromosome evolution shapes sex-dependent asymmetrical introgression barrier

Sex chromosomes play a special role in the evolution of reproductive barriers between species. Here we describe conflicting roles of nascent sex chromosomes on patterns of introgression in an experimental hybrid swarm. Drosophila nasuta and Drosophila albomicans are recently diverged, fully fertile sister species that have different sex chromosome systems. The fusion between an autosome (Muller CD) with the ancestral X and Y gave rise to neo-sex chromosomes in D. albomicans, while Muller CD remains unfused in D. nasuta. We found that a large block containing overlapping inversions on the neo-sex chromosome stood out as the strongest barrier to introgression. Intriguingly, the neo-sex chromosome introgression barrier is asymmetrical and sex-dependent. Female hybrids showed significant D. albomicans–biased introgression on Muller CD (neo-X excess), while males showed heterosis with excessive (neo-X, D. nasuta Muller CD) genotypes. We used a population genetic model to dissect the interplay of sex chromosome drive, heterospecific pairing incompatibility between the neo-sex chromosomes and unfused Muller CD, neo-Y disadvantage, and neo-X advantage in generating the observed sex chromosome genotypes in females and males. We show that moderate neo-Y disadvantage and D. albomicans specific meiotic drive are required to observe female-specific D. albomicans–biased introgression in this system, together with pairing incompatibility and neo-X advantage. In conclusion, this hybrid swarm between a young species pair sheds light onto the multifaceted roles of neo-sex chromosomes in a sex-dependent asymmetrical introgression barrier at a species boundary.

Species Persistence with Hybridization in Toad-Headed Lizards Driven by Divergent Selection and Low Recombination.

Speciation plays a central role in evolutionary studies, and particularly how reproductive isolation (RI) evolves. The origins and persistence of RI are distinct processes that require separate evaluations. Treating them separately clarifies the drivers of speciation and then it is possible to link the processes to understand large-scale patterns of diversity. Recent genomic studies have focused predominantly on how species or RI originate. However, we know little about how species persist in face of gene flow. Here, we evaluate a contact zone of two closely related toad-headed lizards (Phrynocephalus) using a chromosome-level genome assembly and population genomics. To some extent, recent asymmetric introgression from Phrynocephalus putjatai to P. vlangalii reduces their genomic differences. However, their highly divergent regions (HDRs) have heterogeneous distributions across the genomes. Functional gene annotation indicates that many genes within HDRs are involved in reproduction and RI. Compared with allopatric populations, contact areas exhibit recent divergent selection on the HDRs and a lower population recombination rate. Taken together, this implies that divergent selection and low genetic recombination help maintain RI. This study provides insights into the genomic mechanisms that drive RI and two species persistence in the face of gene flow during the late stage of speciation.