Postzygotic Reproductive Isolation Research Articles

Multiple Genomic Landscapes of Recombination and Genomic Divergence in Wild Populations of House Mice-The Role of Chromosomal Fusions and Prdm9.

Chromosomal fusions represent one of the most common types of chromosomal rearrangements found in nature. Yet, their role in shaping the genomic landscape of recombination and hence genome evolution remains largely unexplored. Here, we take advantage of wild mice populations with chromosomal fusions to evaluate the effect of this type of structural variant on genomic landscapes of recombination and divergence. To this aim, we combined cytological analysis of meiotic crossovers in primary spermatocytes with inferred analysis of recombination rates based on linkage disequilibrium using single nucleotide polymorphisms. Our results suggest the presence of a combined effect of Robertsonian fusions and Prdm9 allelic background, a gene involved in the formation of meiotic double strand breaks and postzygotic reproductive isolation, in reshaping genomic landscapes of recombination. We detected a chromosomal redistribution of meiotic recombination toward telomeric regions in metacentric chromosomes in mice with Robertsonian fusions when compared to nonfused mice. This repatterning was accompanied by increased levels of crossover interference and reduced levels of estimated recombination rates between populations, together with high levels of genomic divergence. Interestingly, we detected that Prdm9 allelic background was a major determinant of recombination rates at the population level, whereas Robertsonian fusions showed limited effects, restricted to centromeric regions of fused chromosomes. Altogether, our results provide new insights into the effect of Robertsonian fusions and Prdm9 background on meiotic recombination.

Dysfunction of duplicated pair rice histone acetyltransferases causes segregation distortion and an interspecific reproductive barrier

Postzygotic reproductive isolation, which results in the irreversible divergence of species, is commonly accompanied by hybrid sterility, necrosis/weakness, or lethality in the F1 or other offspring generations. Here we show that the loss of function of HWS1 and HWS2, a couple of duplicated paralogs, together confer complete interspecific incompatibility between Asian and African rice. Both of these non-Mendelian determinants encode the putative Esa1-associated factor 6 (EAF6) protein, which functions as a characteristic subunit of the histone H4 acetyltransferase complex regulating transcriptional activation via genome-wide histone modification. The proliferating tapetum and inappropriate polar nuclei arrangement cause defective pollen and seeds in F2 hybrid offspring due to the recombinant HWS1/2-mediated misregulation of vitamin (biotin and thiamine) metabolism and lipid synthesis. Evolutionary analysis of HWS1/2 suggests that this gene pair has undergone incomplete lineage sorting (ILS) and multiple gene duplication events during speciation. Our findings have not only uncovered a pair of speciation genes that control hybrid breakdown but also illustrate a passive mechanism that could be scaled up and used in the guidance and optimization of hybrid breeding applications for distant hybridization.

Genetic Cause of Hybrid Lethality Observed in Reciprocal Interspecific Crosses between Nicotiana simulans and N. tabacum.

Hybrid lethality, a type of postzygotic reproductive isolation, is an obstacle to wide hybridization breeding. Here, we report the hybrid lethality that was observed in crosses between the cultivated tobacco, Nicotiana tabacum (section Nicotiana), and the wild tobacco species, Nicotiana simulans (section Suaveolentes). Reciprocal hybrid seedlings were inviable at 28 °C, and the lethality was characterized by browning of the hypocotyl and roots, suggesting that hybrid lethality is due to the interaction of nuclear genomes derived from each parental species, and not to a cytoplasmic effect. Hybrid lethality was temperature-sensitive and suppressed at 36 °C. However, when hybrid seedlings cultured at 36 °C were transferred to 28 °C, all of them showed hybrid lethality. After crossing between an N. tabacum monosomic line missing one copy of the Q chromosome and N. simulans, hybrid seedlings with or without the Q chromosome were inviable and viable, respectively. These results indicated that gene(s) on the Q chromosome are responsible for hybrid lethality and also suggested that N. simulans has the same allele at the Hybrid Lethality A1 (HLA1) locus responsible for hybrid lethality as other species in the section Suaveolentes. Haplotype analysis around the HLA1 locus suggested that there are at least six and two haplotypes containing Hla1-1 and hla1-2 alleles, respectively, in the section Suaveolentes.

High sexual display trait diversity without measured genetic divergence in a montane hybrid zone involving young species (Habronattus americanus subgroup, Araneae: Salticidae)

Abstract Genetic introgression, allele exchange across species boundaries, is a commonly recognized feature of animal evolution. Under such a paradigm, contemporary contact zones provide first-hand insight into the geographic, phenotypic, and genetic details of introgression. Also, when mate choice phenotypes are conspicuous and variable in hybrids, contact zones provide potential insight into how sexual selection interacts with species boundary maintenance, particularly when postzygotic reproductive isolation is weak. The Habronattus americanus subgroup includes several recently evolved jumping spider species, with an estimated age of about 200,000 yr, and substantial evidence for hybridization and introgression. We explored a contact zone involving H. americanus (Keyserling, 1885) and H. kubai (Griswold, 1979) on Mount Shasta, CA, in alpine habitats that would have been unavailable (under ice) at the Last Glacial Maximum. We characterized morphological diversity within the contact zone, including the fine-scale geographic distribution of hybrid and parental individuals, and assessed genetic variation using ddRADseq data. Combined results indicate a lack of measured genomic differentiation between specimens with distinct morphologies, including individuals with phenotypes of the parental species. We identified a diverse array of hybrid morphologies, with phenotypic evidence for backcrossing, essentially forming a phenotypic bridge between parental taxa. The study area is characterized by more hybrid than parental individuals, with a significantly larger number of red-palped morphologies than white- and/or yellow-palped morphologies; the novel, white-palped phenotype is perhaps transgressive. Overall, these results contribute to a better understanding of the expected ebb and flow of lineage interactions during the early stages of speciation.

Patterns of speciation in a parapatric pair of Saturnia moths as revealed by target capture.

The focus of this study has been to understand the evolutionary relationships and taxonomy of a widely distributed parapatric species pair of wild silk moths in Europe: Saturnia pavonia and Saturnia pavoniella (Lepidoptera: Saturniidae). To address species delimitation in these parapatric taxa, target enrichment and mtDNA sequencing was employed alongside phylogenetic, admixture, introgression, and species delimitation analyses. The dataset included individuals from both species close to and farther away from the contact zone as well as two hybrids generated in the lab. Nuclear markers strongly supported both S. pavonia and S. pavoniella as two distinct species, with hybrids forming a sister group to S. pavoniella. However, the Maximum Likelihood (ML) tree generated from mtDNA sequencing data presented a different picture, showing both taxa to be phylogenetically intermixed. This inconsistency is likely attributable to mitonuclear discordance, which can arise from biological factors (e.g., introgressive hybridization and/or incomplete lineage sorting). Our analyses indicate that past introgressions have taken place, but that there is no evidence to suggest an ongoing admixture between the two species, demonstrating that the taxa have reached full postzygotic reproductive isolation and hence represent two distinct biological species. Finally, we discuss our results from an evolutionary point of view taking into consideration the past climatic oscillations that have likely shaped the present dynamics between the two species. Overall, our study demonstrates the effectiveness of the target enrichment approach in resolving shallow phylogenetic relationships under complex evolutionary circumstances and that this approach is useful in establishing robust and well-informed taxonomic delimitations involving parapatric taxa.

Domestication is associated with increased interspecific hybrid compatibility in landfowl (order: Galliformes).

Some species are able to hybridize despite being exceptionally diverged. The causes of this variation in accumulation of reproductive isolation remain poorly understood, and domestication as an impetus or hindrance to reproductive isolation remains to be characterized. In this study, we investigated the role of divergence time, domestication, and mismatches in morphology, habitat, and clutch size among hybridizing species on reproductive isolation in the bird order Galliformes. We compiled and analyzed hybridization occurrences from literature and recorded measures of postzygotic reproductive isolation. We used a text-mining approach leveraging a historical aviculture magazine to quantify the degree of domestication across species. We obtained divergence time, morphology, habitat, and clutch size data from open sources. We found 123 species pairs (involving 77 species) with known offspring fertility (sterile, only males fertile, or both sexes fertile). We found that divergence time and clutch size were significant predictors of reproductive isolation (McFadden's Pseudo-R2 = 0.59), but not habitat or morphological mismatch. Perhaps most interesting, we found a significant relationship between domestication and reproductive compatibility after correcting for phylogeny, removing extreme values, and addressing potential biases (F1,74 = 5.43, R2 = 0.06, P-value = 0.02). We speculate that the genetic architecture and disruption in selective reproductive regimes associated with domestication may impact reproductive isolation, causing domesticated species to be more reproductively labile.

Diversifying selection in aly, bam, dj and topi genes: Association between Rapid divergence and Hybrid male sterility in Drosophila bipectinata species complex

The diversity of millions of species depends on the multiplication of species and speciation, in which reproductive isolation evolves, such as hybrid sterility: a puzzle that still remains unknown. Crosses between closely related species results in sterile hybrid males, the perturbances of spermatogenesis in the F1 hybrid males usually affect the later stages of development, arresting at the sperm individualization stage, which could be due to the rapid interspecies divergence of reproductive genes experiencing strong selective constraints between species. We annotated and analyzed the molecular evolution of 6 key spermatogenesis genes playing an important role in the sperm developmental pathway in 15 strains of Drosophila bipectinata species subcomplex, where the interspecies crosses are known to produce sterile hybrid males. We analyzed nucleotide divergence and characterized the patterns of sequence polymorphism in the protein-coding regions to validate or reject the nature of adaptive divergence using its phylogenetic histories. Except for spermatocyte arrest (sa) and twine, all 4 genes - always early(aly), bag of marbles(bam), don juan (dj) and matotopetli (topi) showed signatures of positive selection with more nonsynonymous to synonymous fixed differences between species. However, departure from neutrality in polymorphism analysis was only significant for topi, twine and aly. Consistent with our analysis proving rapid divergence of don juan(dj) and topi, hybrids involving the three species Drosophila bipectinata, Drosophila parabipectinata and Drosophila malerkotliana, have found immotile sperm and unindividualized spermatids. Bag of marbles(bam) and aly showed rapid divergence coherent to the aspermic testes abnormality found in the hybrid males from crosses involving the Drosophila pseudoananassae with the other three species. We propose that faster evolution of spermatogenesis genes due to a yet unknown underlying mechanism acting upon the germ cell line developmental pathway of these four species might be operating as a perpetual dynamo for interspecies divergence and hybrid male sterility. Our study is the first attempt to understand the molecular genetic basis of post-zygotic reproductive isolation in bipectinata species complex and lays a foundation for future detailed exploration to better understand the mechanisms involved.

Hybridization in late stages of speciation: Strong but incomplete genome-wide reproductive isolation and 'large Z-effect' in a moving hybrid zone.

In organisms reproducing sexually, speciation occurs when increasing divergence results in pre- or post-zygotic reproductive isolation between lineages. Studies focusing on reproductive isolation origin in early stages of speciation are common and many rely on genomic scans to infer introgression providing limited information on the genomic architecture of reproductive isolation long-term maintenance. This study analyses a natural hybrid zone between two species in a late stage of speciation. We used ddRADseq genotyping in the contact between Podarcis bocagei and P. carbonelli to examine admixture extent, analyse hybrid zone stability and assess genome-wide variation in selection against introgression. We confirmed strong but incomplete reproductive isolation in a bimodal hybrid zone. New findings revealed population genetic structure within P. carbonelli in the contact zone; geographical and genomic clines analysis suggested strong selection against gene flow, but a relatively small proportion of the loci can introgress, mostly within the narrow contact zone. However, geographical clines revealed that a few introgressed loci show signs of potential positive selection, particularly into P. bocagei. Geographical clines also detected a signal of hybrid zone movement towards P. bocagei distribution. Genomic cline analysis revealed heterogeneous patterns of introgression among loci within the syntopy zone, but the majority maintain a strong association with the genomic background of origin. However, incongruences between both cline approaches were found, potentially driven by confounding effects on genomic clines. Last, an important role of the Z chromosome in reproductive isolation is suggested. Importantly, overall patterns of restricted introgression seem to result from numerous strong intrinsic barriers across the genome.

Evolution of reproductive isolation in a long-term evolution experiment with Drosophila melanogaster: 30 years of divergent life-history selection.

We ask if three decades and over 1,500 generations of divergent life-history selection on age at reproduction has resulted in the evolution of reproductive isolation (RI) between laboratory populations of Drosophila melanogaster. We tested for premating, postmating-prezygotic, and postzygotic reproductive isolation between three replicate population pairs. Large, evolved differences in body size between selection treatments suggested the potential for prezygotic barriers driven by sexual selection or physical incompatibilities between the sexes. Although a simple prediction would be preference for larger size, creating directional isolation, our results from individual mate choice trials indicate that populations from both selection treatments show a marked bias towards homotypic mate choice; indicative of prezygotic RI driven by sexual selection or sexual conflict. Hybridization between the focal populations resulted in the production of viable adult flies with intermediate size and developmental traits. We observed a suggestive but statistically nonsignificant trend of fitness decline in the F2 generation of hybrids, but no significant evidence suggesting the evolution of postmating-prezygotic or postzygotic RI. Our findings are in accord with extant literature that posits that premating RI evolves before postmating forms of RI.

Regulatory Divergence as a Mechanism for X-Autosome Incompatibilities in Caenorhabditis Nematodes.

The world's astounding biodiversity results from speciation, the process of formation of distinct species. Hybrids between species often have reduced fitness due to negative epistatic interactions between divergent genetic factors, as each lineage accumulated substitutions independently in their evolutionary history. Such negative genetic interactions can manifest as gene misexpression due to divergence in gene regulatory controls from mutations in cis-regulatory elements and trans-acting factors. Gene misexpression due to differences in regulatory controls can ultimately contribute to incompatibility within hybrids through developmental defects such as sterility and inviability. We sought to quantify the contributions of regulatory divergence to postzygotic reproductive isolation using sterile interspecies hybrids of two Caenorhabditis nematodes: Caenorhabditis briggsae and Caenorhabditis nigoni. We analyzed previous transcriptome profiles for two introgression lines with distinct homozygous X-linked fragments from C. briggsae in a C. nigoni genomic background that confers male sterility, owing to defects in spermatogenesis (Li R, et al. 2016. Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-chromosome introgression. Genome Res. 26:1219-1232). Our analysis identified hundreds of genes that show distinct classes of nonadditive expression inheritance and regulatory divergence. We find that these nonoverlapping introgressions affect many of the same genes in the same way and demonstrate that the preponderance of transgressive gene expression is due to regulatory divergence involving compensatory and joint effects of cis- and trans-acting factors. The similar transcriptomic responses to nonoverlapping genetic perturbations of the X-chromosome implicate multiway incompatibilities as an important feature contributing to hybrid male sterility in this system.

Meiotic Recognition of Evolutionarily Diverged Homologs: Chromosomal Hybrid Sterility Revisited.

Hybrid sterility (HS) is an early postzygotic reproductive isolation mechanism observed in all sexually reproducing species. Infertility of hybrids prevents gene flow between incipient species and leads to speciation. While Drosophila studies have focused almost exclusively on the genic control of HS, two other model species, Mus musculus and budding yeast, provided the first experimental evidence of hybrid sterility governed by the nongenic effects of DNA sequence divergence. Here, we propose that the nongenic effect of increasing DNA divergence between closely related species may impair mutual recognition of homologous chromosomes and disrupt their synapsis. Unsynapsed or mispaired homologs can induce early meiotic arrest, or their random segregation can cause aneuploidy of spermatids and sperm cells. Impaired recognition of homologs may thus act as a universal chromosomal checkpoint contributing to the complexity of genetic control of HS. Chromosomal HS controlled by the Prdm9 gene in mice and HS driven by the mismatch repair machinery in yeast are currently the most advanced examples of chromosomal homology search-based HS. More focus on the cellular and molecular phenotypes of meiosis will be needed to further validate the role of homolog recognition in hybrid sterility and speciation.

Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak

BackgroundInterspecific hybridization plays vital roles in enriching animal diversity, while male hybrid sterility (MHS) of the offspring commonly suffered from spermatogenic arrest constitutes the postzygotic reproductive isolation. Cattle-yak, the hybrid offspring of cattle (Bos taurus) and yak (Bos grunniens) can serve as an ideal MHS animal model. Although meiotic arrest was found to contribute to MHS of cattle-yak, yet the cellular characteristics and developmental potentials of male germline cell in pubertal cattle-yak remain to be systematically investigated.ResultsSingle-cell RNA-seq analysis of germline and niche cell types in pubertal testis of cattle-yak and yak indicated that dynamic gene expression of developmental germ cells was terminated at late primary spermatocyte (meiotic arrest) and abnormal components of niche cell in pubertal cattle-yak. Further in vitro proliferation and differentially expressed gene (DEG) analysis of specific type of cells revealed that undifferentiated spermatogonia of cattle-yak exhibited defects in viability and proliferation/differentiation potentials.ConclusionComparative scRNA-seq and in vitro proliferation analysis of testicular cells indicated that not only meiotic arrest contributed to MHS of cattle-yak. Spermatogenic arrest of cattle-yak may originate from the differentiation stage of undifferentiated spermatogonia and niche cells of cattle-yak may provide an adverse microenvironment for spermatogenesis.

Experimental Crosses Between Two Dung Beetle Lineages Show Transgressive Segregation in Physiological Traits

Physiological traits in insects are intrinsically related to their behavior, fitness,and survival and can reflect adaptations to ecological stressors in different environments, leading to population differentiation that may cause hybrid failure. In this study,we characterized five physiological traits related to body condition (body size, body mass, amount of fat, total hemolymph protein, and phenoloxidase activity) in twogeographically separated andrecently differentiated lineages ofCanthon cyanellusLeConte, 1859 within their natural distribution in Mexico. We also performed experimental hybrid crosses between these lineages tobetter understand the differentiation process and explore the presence of transgressive segregation over physiological traitsin them. We found differences between lineages in all traits except body mass,suggestingselective pressuresrelated todifferent ecological pressures. Thesedifferences werealsoapparent in the transgressive segregation of all traits in F1 and F2 hybrids,except for phenoloxidase activity.Protein content was sexually dimorphic in both parental lineages but was reversed in hybrids, suggesting a genetic basis for the differences between sexes.The negative sign of transgressive segregation for most traitsindicatesthat hybrids wouldbe smaller, thinner,and generallyunfit. Our results suggest thatthese twolineages may undergo postzygotic reproductive isolation, confirming the cryptic diversity of this species complex.

Multiple pre- and postzygotic components of reproductive isolation between two co-occurring Lysimachia species.

Genetic divergence between species depends on reproductive isolation (RI) due to traits that reduce interspecific mating (prezygotic isolation) or are due to reduced hybrid fitness (postzygotic isolation). Previous research found that prezygotic barriers tend to be stronger than postzygotic barriers, but most studies are based on the evaluation of F1 hybrid fitness in early life cycle stages. We combined field and experimental data to determine the strength of 17 prezygotic and postzygotic reproductive barriers between two Lysimachia species that often co-occur and share pollinators. We assessed postzygotic barriers up to F2 hybrids and backcrosses. The two species showed near complete RI due to the cumulative effect of multiple barriers, with an uneven and asymmetric contribution to isolation. In allopatry, prezygotic barriers contributed more to reduce gene flow than postzygotic barriers, but their contributions were more similar in sympatry. The strength of postzygotic RI was up to three times lower for F1 progeny than for F2 or backcrossed progenies, and RI was only complete when late F1 stages and either F2 or backcrosses were accounted for. Our results thus suggest that the relative strength of postzygotic RI may be underestimated when its effects on late stages of the life cycle are disregarded.

Karyotype evolution in Ronderosia grasshoppers (Orthoptera: Acrididae)

Abstract Grasshoppers in the genus Ronderosia (divergence time < 5 Mya) provide a special opportunity to examine the impact of chromosome rearrangements (CRs) in evolution and speciation, because they exhibit extensively rearranged karyotypes involving autosome-autosome and autosome-X chromosomes, the latter leading to the formation of a neo-sex chromosome system (neo-SCS). Despite the potential role of CRs in speciation, the general patterns of karyotype changes resulting from CRs in Ronderosia are still unclear. Here we investigated karyotype evolution in eight Ronderosia species using cytogenetic and phylogenetic models of ancestral character reconstruction. The overall findings suggest a central role for CRs in generating variability in chromosome number and neo-SCS across Ronderosia grasshoppers. It also suggests that incipient species with little morphological change, such as those observed in Ronderosia species, could accumulate marked differences in their karyotypes contributing to post-zygotic reproductive isolation. Besides the evolution of chromosome number in the phylogeny of the genus, chromosome change due to centric fusion is coupled with the divergence pattern observed in the group. While a cladogenetic event could represent a case where karyotypic differences result in speciation, further in-depth genomic studies are needed to better understand how these dramatic restructurings of karyotypes may have occurred.

Reproductive isolation between diploid and tetraploid individuals in mixed‐cytotype populations of Lycium australe

Whole-genome duplication is considered a major mechanism of sympatric speciation due to the creation of strong and instantaneous reproductive barriers. Although postzygotic reproductive isolation between diploids and polyploids is often expected, the extent of reproductive incompatibility must be empirically determined and compared to patterns of genetic isolation to fully characterize the reproductive dynamics between cytotypes. We investigated reproductive compatibility between diploid and tetraploid Lycium australe in two mixed-cytotype populations using (1) controlled crossing experiments to evaluate fruit and seed production and (2) germination trials to test seed viability following homoploid and heteroploid crosses. We contrast these experiments with a single-nucleotide polymorphism (SNP) data set to measure genetic isolation between cytotypes and explore whether cytotype or population origin better explains patterns of genetic variation. Finally, we explore mating patterns using the observed germination rates of naturally produced seeds in each population. Although homoploid and heteroploid crosses resulted in similar fruit and seed production, reproductive isolation between co-occurring diploids and tetraploids was nearly complete, due to low seed viability following heteroploid crosses. Of 191,182 total SNPs, 21,679 were present in ≥90% of individuals and replicate runs using unlinked SNPs revealed strong clustering by cytotype and differentiation of tetraploids based on population origin. As often reported, diploid and tetraploid L. australe experience strong postzygotic isolation via hybrid seed inviability. Consistent with this result, cytotype explained a greater amount of variation in the SNP data set than population origin, despite some evidence of historical introgression.

Intraspecific variation in reproductive barriers between two closely related Arabidopsis sister species.

Reproductive isolation (RI) is a critical component of speciation and varies strongly in timing and strength among different sister taxa, depending on, for example the geography of speciation and divergence time. However, these factors may also produce variation in timing and strength among populations within species. Here we tested for variation in the expression of RI among replicate population pairs between the sister taxa Arabidopsis lyrata subsp. lyrata and A. arenicola. While the former is predominantly outcrossing, the latter is predominantly selfing. We focused on intrinsic prezygotic and postzygotic RI as both species occur largely in allopatry. We assessed RI by performing within-population crosses and interspecific between-population crosses, and by raising offspring. RI was generally high between all interspecific population pairs, but it varied in timing and strength depending on population history. Prezygotic isolation was strongest between the closest-related population pair, while early postzygotic isolation was high for all other population pairs. Furthermore, the timing and strength of RI depended strongly on cross direction. Our study provides empirical support that reproductive barriers between species are highly variable among population pairs and asymmetric within population pairs, and this variation seems to follow patterns typically described across species pairs.

Revisiting the Genetic, Taxonomic and Evolutionary Aspects of Chagas Disease Vectors of the Triatoma phyllosoma Subcomplex (Hemiptera, Triatominae)

Triatoma bassolsae, T. longipennis, T. mazzottii, T. pallidipennis, T. phyllosoma and T. picturata are species that have great epidemiological importance in the transmission of Chagas disease in Mexico. However, there is no consensus regarding the specific status of these species, since they appear in various articles as species, subspecies and even subgenera. Thus, we revisited genetic, taxonomic and evolutionary data that allowed us to assess and discuss the specific status of these six species of the T. phyllosoma subcomplex. Phylogenetic studies were performed with nuclear (18S, 28S, ITS-2) and mitochondrial (16S, cytb, COI, COII, 12S) markers deposited in GenBank. In addition, data from experimental crosses were pooled and the genetic distance to the cytb gene was calculated. The phylogenetic reconstruction enabled us to rescue the six species as independent lineages. Post-zygotic reproductive isolation barriers (sterility and/or hybrid collapse) were observed for some experimental crosses. Although the other experimental crosses did not allow us to characterize reproductive barriers, these species showed high genetic distances in relation to the cytb gene (ranging from 4.6% to 14.9%). Thus, based on the revisited literature data, we confirmed the specific status of these six species of the T. phyllosoma subcomplex based on the phylogenetic and biological concepts of the species.

Host-plant adaptation as a driver of incipient speciation in the fall armyworm (Spodoptera frugiperda)

BackgroundDivergent selection on host-plants is one of the main evolutionary forces driving ecological speciation in phytophagous insects. The ecological speciation might be challenging in the presence of gene flow and assortative mating because the direction of divergence is not necessarily the same between ecological selection (through host-plant adaptation) and assortative mating. The fall armyworm (FAW), a major lepidopteran pest species, is composed of two sympatric strains, corn and rice strains, named after two of their preferred host-plants. These two strains have been hypothesized to undergo incipient speciation, based on (i) several lines of evidence encompassing both pre- and post-zygotic reproductive isolation, and (ii) the presence of a substantial level of genetic differentiation. Even though the status of these two strains has been established a long time ago, it is still yet to be found whether these two strains indeed exhibit a marked level of genetic differentiation from a large number of genomic loci. Here, we analyzed whole genome sequences from 56 FAW individuals either collected from pasture grasses (a part of the favored host range of the rice strain) or corn to assess the role of host-plant adaptation in incipient speciation.ResultsPrincipal component analysis of whole genome data shows that the pattern of divergence in the fall armyworm is predominantly explained by the genetic differentiation associated with host-plants. The level of genetic differentiation between corn and rice strains is particularly marked in the Z chromosome. We identified one autosomal locus and two Z chromosome loci targeted by selective sweeps specific to rice strain and corn strain, respectively. The autosomal locus has both increased DXY and FST while the Z chromosome loci had decreased DXY and increased FST.ConclusionThese results show that the FAW population structure is dominated by the genetic differentiation between corn and rice strains. This differentiation involves divergent selection targeting at least three loci, which include a locus potentially causing reproductive isolation. Taken together, these results suggest the evolutionary scenario that host-plant speciation is a driver of incipient speciation in the fall armyworm.

Enforcement of Postzygotic Species Boundaries in the Fungal Kingdom.

Understanding the molecular basis of speciation is a primary goal in evolutionary biology. The formation of the postzygotic reproductive isolation that causes hybrid dysfunction, thereby reducing gene flow between diverging populations, is crucial for speciation. Using various advanced approaches, including chromosome replacement, hybrid introgression and transcriptomics, population genomics, and experimental evolution, scientists have revealed multiple mechanisms involved in postzygotic barriers in the fungal kingdom. These results illuminate both unique and general features of fungal speciation. Our review summarizes experiments on fungi exploring how Dobzhansky-Muller incompatibility, killer meiotic drive, chromosome rearrangements, and antirecombination contribute to postzygotic reproductive isolation. We also discuss possible evolutionary forces underlying different reproductive isolation mechanisms and the potential roles of the evolutionary arms race under the Red Queen hypothesis and epigenetic divergence in speciation.