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Evaluating the fitness of hybrids can provide important insights into genetic differences between species or diverging populations. We focused on surface- and cave-ecotypes of the widespread Atlantic molly Poecilia mexicana and raised F1 hybrids of reciprocal crosses to sexual maturity in a common-garden experiment. Hybrids were reared in a fully factorial 2 × 2 design consisting of lighting (light vs. darkness) and resource availability (high vs. low food). We quantified survival, ability to realize their full reproductive potential (i.e., completed maturation for males and 3 consecutive births for females) and essential life-history traits. Compared to the performance of pure cave and surface fish from a previous experiment, F1s had the highest death rate and the lowest proportion of fish that reached their full reproductive potential. We also uncovered an intriguing pattern of sex-specific phenotype expression, because male hybrids expressed cave molly life histories, while female hybrids expressed surface molly life histories. Our results provide evidence for strong selection against hybrids in the cave molly system, but also suggest a complex pattern of sex-specific (opposing) dominance, with certain surface molly genes being dominant in female hybrids and certain cave molly genes being dominant in male hybrids.

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To explain how populations with distinct warning signals coexist in close parapatry, we experimentally assessed intrinsic mechanisms acting as reproductive barriers within three poison-frog species from the Peruvian Amazon belonging to a Müllerian mimetic ring (Ranitomeya variabilis, Ranitomeya imitator and Ranitomeya fantastica). We tested the role of prezygotic and postzygotic isolation barriers between phenotypically different ecotypes of each species, using no-choice mating experiments and offspring survival analysis. Our results show that prezygotic mating preference did not occur except for one specific ecotype of R. imitator, and that all three species were able to produce viable inter-population F1 hybrids. However, while R. variabilis and R. imitator hybrids were able to produce viable F2 generations, we found that for R. fantastica, every F1 hybrid males were sterile while females remained fertile. This unexpected result, echoing with Haldane's rule of speciation, validated phylogenetic studies which tentatively diagnose these populations of R. fantastica as two different species. Our work suggests that postzygotic genetic barriers likely participate in the extraordinary phenotypic diversity observed within Müllerian mimetic Ranitomeya populations, by maintaining species boundaries.

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Hybridization plays a pivotal role in evolution, influencing local adaptation and speciation. However, it can also reduce biodiversity, which is especially damaging when native and non-native species meet. Hybridization can threaten native species via competition (with vigorous hybrids), reproductive resource wastage and gene introgression. The latter, in particular, could result in increased fitness in invasive species, decreased fitness of natives and compromise reintroduction or recovery conservation practices. In this study, we use a combination of RAD sequencing and microsatellites for a range-wide sample set of 1366 fish to evaluate the potential for hybridization and introgression between native crucian carp (Carassius carassius) and three non-native taxa (Carassius auratus auratus, Carassius auratus gibelio and Cyprinus carpio) in European water bodies. We found hybridization between native and non-native taxa in 82% of populations with non-natives present, highlighting the potential for substantial ecological impacts from hybrids on crucian carp populations. However, despite such high rates of hybridization, we could find no evidence of introgression between these taxa. The presence of triploid backcrosses in at least two populations suggests that the lack of introgression among these taxa is likely due to meiotic dysfunction in hybrids, leading to the production of polyploid offspring which are unable to reproduce sexually. This result is promising for crucian reintroduction programs, as it implies limited risk to the genetic integrity of source populations. Future research should investigate the reproductive potential of triploid hybrids and the ecological pressures hybrids impose on C. carassius.

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Interspecies hybrid sterility has been extensively studied, especially in the genus Drosophila. Hybrid sterility is more often found in the heterogametic (XY or ZW) sex, a trend called Haldane's rule. Although this phenomenon is pervasive, identification of a common genetic mechanism remains elusive, with modest support found for a range of potential theories. Here, we identify a single precise morphological phenotype, which we call 'needle-eye sperm', that is associated with hybrid sterility in three separate species pairs that span the Drosophila genus. The nature of the phenotype indicates a common point of meiotic failure in sterile hybrid males. We used 10 generations of backcross selection paired with whole-genome pooled sequencing to genetically map the regions underlying the needle-eye (NE) sperm phenotype. Surprisingly, the sterility phenotype was present in ~50% of males even after 10 generations of backcrossing, and only a single region of the X chromosome was associated with sterility in one direction of backcross. Owing to the common phenotype among sterile male hybrids, and the strong effect of individual loci, further exploration of these findings may identify a universal mechanism for the evolution of hybrid sterility.

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AbstractHaldane's rule-a pattern in which hybrid sterility or inviability is observed in the heterogametic sex of an interspecific cross-is one of the most widely obeyed rules in nature. Because inheritance patterns are similar for sex chromosomes and haplodiploid genomes, Haldane's rule may apply to haplodiploid taxa, predicting that haploid male hybrids will evolve sterility or inviability before diploid female hybrids. However, there are several genetic and evolutionary mechanisms that may reduce the tendency of haplodiploids to obey Haldane's rule. Currently, there are insufficient data from haplodiploids to determine how frequently they adhere to Haldane's rule. To help fill this gap, we crossed a pair of haplodiploid hymenopteran species (Neodiprion lecontei and Neodiprion pinetum) and evaluated the viability and fertility of female and male hybrids. Despite considerable divergence, we found no evidence of reduced fertility in hybrids of either sex, consistent with the hypothesis that hybrid sterility evolves slowly in haplodiploids. For viability, we found a pattern opposite to that of Haldane's rule: hybrid females, but not males, had reduced viability. This reduction was most pronounced in one direction of the cross, possibly due to a cytoplasmic-nuclear incompatibility. We also found evidence of extrinsic postzygotic isolation in hybrids of both sexes, raising the possibility that this form or reproductive isolation tends to emerge early in speciation in host-specialized insects. Our work emphasizes the need for more studies on reproductive isolation in haplodiploids, which are abundant in nature but underrepresented in the speciation literature.

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Postmating isolation is thought to be an important driver of the late stages of speciation. However, relatively little is empirically known about the process compared with other isolating mechanisms that drive the early stages of speciation, especially in non-model organisms. We characterized the genetic architecture of postmating isolation between 2 rockfishes, Sebastes schlegelii and S. trivittatus, whose reproductive isolation is complete. We examined transmission ratio distortion (TRD) patterns of genetic markers in 2 reciprocal backcross populations. Markers showing either of the 2 types of TRD was widespread across the genome, with some of the distorted markers forming extensive clusters around the recombination coldspots. These suggest that the postmating isolation effectively prevents gene flow across the genome and the recombination landscape contributes to the genetic architecture. Comparisons between 2 backcross families and 2 developmental stages showed little similarity in the distorted markers, suggesting asymmetry and stage specificity of the isolation. This may be due to hybrid incompatibility involving maternal factors or extrinsic selection. The lack of sex-ratio distortion in the mapping families suggested that Haldane's rule in terms of hybrid inviability does not hold. Additionally, quantitative trait loci (QTL) mapping detected significant QTLs for sex and the morphological traits relevant to speciation and convergence of rockfishes, including body coloration. Genes in the melanocortin system, including agouti-signaling protein 1 (asip1) and melanocortin 1 receptor (mc1r), might underlie the horizontal and vertical color patterns on the body, respectively. These findings constitute an essential step toward a comprehensive understanding of speciation and morphological diversification of rockfishes.

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Haldane's rule is one of the 'two rules of speciation'. It states that if one sex is 'absent, rare or sterile' in a hybrid population, then that sex will be heterogametic. Since Haldane first made this observation, 100 years have passed and still questions arise over how many independent examples exist and what the underlying causes of Haldane's rule are. This review aims to examine research that has occurred over the last century. It seeks to do so by discussing possible causes of Haldane's rule, as well as gaps in the research of these causes that could be readily addressed today. After 100 years of research, it can be concluded that Haldane's rule is a complicated one, and much current knowledge has been accrued by studying the model organisms of speciation. This has led to the primacy of dominance theory and faster-male theory as explanations for Haldane's rule. However, some of the most interesting findings of the 21st century with regard to Haldane's rule have involved investigating a wider range of taxa emphasizing the need to continue using comparative methods, including ever more taxa as new cases are discovered.

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Genetic divergence among allopatric populations builds reproductive isolation over time. This process is accelerated when populations face a changing environment that allows large-effect mutational differences to accumulate, but abrupt change also places populations at risk of extinction. Here we use simulations of Fisher's geometric model with explicit population dynamics to explore the genetic changes that occur in the face of environmental changes. Because evolutionary rescue leads to the fixation of mutations whose phenotypic effects are larger on average compared with populations not at risk of extinction, these mutations are thus more likely to lead to reproductive isolation. We refer to the formation of new species from the ashes of populations in decline as the phoenix hypothesis of speciation. The phoenix hypothesis predicts more substantial hybrid fitness breakdown among populations surviving a higher extinction risk. The hypothesis was supported when many loci underlie adaptation. With only a small number of potential rescue mutations, however, mutations that fixed in different populations were more likely to be identical, with such parallel changes reducing isolation. Consequently, reproductive isolation builds fastest in populations subject to an intermediate extinction risk, given a limited number of mutations available for adaptation.

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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.

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Crosses between the wild tomato species Solanum peruvianum and Solanum chilense result in hybrid seed failure (HSF), characterized by endosperm misdevelopment and embryo arrest. We previously showed that genomic imprinting, the parent-of-origin-dependent expression of alleles, is perturbed in the hybrid endosperm, with many of the normally paternally expressed genes losing their imprinted status. Here, we report transcriptome-based analyses of gene and small RNA (sRNA) expression levels. We identified 2,295 genes and 387 sRNA clusters as differentially expressed when comparing reciprocal hybrid seed to seeds and endosperms from the two within-species crosses. Our analyses uncovered a pattern of overdominance in endosperm gene expression in both hybrid cross directions, in marked contrast to the patterns of sRNA expression in whole seeds. Intriguingly, patterns of increased gene expression resemble the previously reported increased maternal expression proportions in hybrid endosperms. We identified physical clusters of sRNAs; differentially expressed sRNAs exhibit reduced transcript abundance in hybrid seeds of both cross directions. Moreover, sRNAs map to genes coding for key proteins involved in epigenetic regulation of gene expression, suggesting a regulatory feedback mechanism. We describe examples of genes that appear to be targets of sRNA-mediated gene silencing; in these cases, reduced sRNA abundance is concomitant with increased gene expression in hybrid seeds. Our analyses also show that S. peruvianum dominance impacts gene and sRNA expression in hybrid seeds. Overall, our study indicates roles for sRNA-mediated epigenetic regulation in HSF between closely related wild tomato species.

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Cellular energy production requires coordinated interactions between genetic components from the nuclear and mitochondrial genomes. This coordination results in coadaptation of interacting elements within populations. Interbreeding between divergent gene pools can disrupt coadapted loci and result in hybrid fitness breakdown. While specific incompatible loci have been detected in multiple eukaryotic taxa, the extent of the nuclear genome that is influenced by mitonuclear coadaptation is not clear in any species. Here, we used F2 hybrids between two divergent populations of the copepod Tigriopus californicus to examine mitonuclear coadaptation across the nuclear genome. Using developmental rate as a measure of fitness, we found that fast-developing copepods had higher ATP synthesis capacity than slow developers, suggesting variation in developmental rates is at least partly associated with mitochondrial dysfunction. Using Pool-seq, we detected strong biases for maternal alleles across 7 (of 12) chromosomes in both reciprocal crosses in high-fitness hybrids, whereas low-fitness hybrids showed shifts toward the paternal population. Comparison with previous results on a different hybrid cross revealed largely different patterns of strong mitonuclear coadaptation associated with developmental rate. Our findings suggest that functional coadaptation between interacting nuclear and mitochondrial components is reflected in strong polygenic effects on this life-history phenotype, and reveal that molecular coadaptation follows independent evolutionary trajectories among isolated populations.

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When differentiated lineages come into contact, their fates depend on demographic and reproductive factors. These factors have been well-studied in taxa of the same ploidy, but less is known about sympatric lineages that differ in ploidy, particularly with respect to demographic factors. We assessed prezygotic, postzygotic, and total reproductive isolation in naturally pollinated arrays of diploid-tetraploid and tetraploid-hexaploid population mixes of Campanula rotundifolia by measuring pollinator transitions, seed yield, germination rate, and proportion of hybrid offspring. Four frequencies of each cytotype were tested, and pollinators consistently overvisited rare cytotypes. Seed yield and F1 hybrid production were greater in 4X-6X arrays than 2X-4X arrays, whereas germination rates were similar, creating two distinct patterns of reproductive isolation. In 2X-4X arrays, postzygotic isolation was near complete (3% hybrid offspring), and prezygotic isolation associated with pollinator preference is expected to facilitate the persistence of minority cytotypes. However, in 4X-6X arrays where postzygotic isolation permitted hybrid formation (44% hybrids), pollinator behavior drove patterns of reproductive isolation, with rare cytotypes being more isolated and greater gene flow expected from rare into common cytotypes. In polyploid complexes, both the specific cytotypes in contact and local cytotype frequency, likely reflecting spatial demography, will influence likelihood of gene exchange.

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Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky-Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that many incipient species may initially face. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically interacting mutations that is sufficient to confer strong reproductive isolation. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

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The origins of novel trophic specialization, in which organisms begin to exploit resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics among species. We investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while they consumed shrimp and scales in the lab, and found that scale-eating pupfish exhibited peak gape sizes twice as large as in other species, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring bite size (surface area removed) from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in approximately 40% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale biting. To test whether feeding performance could contribute to reproductive isolation between species, we also measured F1 hybrids and found that their kinematics and performance more closely resembled generalists, suggesting that F1 hybrids may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale eating.

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When two species interbreed, the resulting hybrid offspring are often sterile, with the heterogametic (e.g. XY) hybrid usually being more severely affected. The prevailing theory for this pattern of sterility evokes divergent changes in separate lineages having maladaptive interactions when placed together in a hybrid individual, with recessive factors on the sex chromosome interacting with dominant factors on the autosomes. The effect of these interactions on gametogenesis should not be uniform across species pairs unless genetic divergence follows the same paths in different lineages or if a specific stage of gametogenesis is more susceptible to detrimental genetic interactions. Here, we perform a detailed cellular characterization of hybrid male sterility across three recently diverged species pairs of Drosophila. Across all three pairs, sterile hybrid sperm are alive but exhibit rapid nuclear de-condensation with age, with active, but non-differentiated, mitochondria. Surprisingly, all three sets of interspecies hybrids produce half of the number of sperm per round of spermatogenesis, with each sperm cell containing two tails. We identify non-disjunction failures during meiosis I as the likely cause. Thus, errors during meiosis I may be a general phenomenon underlying Drosophila male sterility, indicating either a heightened sensitivity of this spermatogenic stage to failure, or a basis to sterility other than the prevailing model.

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Comparative genomic approaches are increasingly being used to study the evolution of reproductive barriers in nonmodel species. Although numerous studies have examined prezygotic isolation in darters (Percidae), investigations into postzygotic barriers have remained rare due to long generation times and a lack of genomic resources. Orangethroat and rainbow darters naturally hybridize and provide a remarkable example of male-driven speciation via character displacement. Backcross hybrids suffer from high mortality, which appears to promote behavioral isolation in sympatry. To investigate the genomic architecture of postzygotic isolation, we used Illumina and PacBio sequencing to generate a chromosome-level, annotated assembly of the orangethroat darter genome and high-density linkage maps for orangethroat and rainbow darters. We also analyzed genome-wide RADseq data from wild-caught adults of both species and laboratory-generated backcrosses to identify genomic regions associated with hybrid incompatibles. Several putative chromosomal translocations and inversions were observed between orangethroat and rainbow darters, suggesting structural rearrangements may underlie postzygotic isolation. We also found evidence of selection against recombinant haplotypes and transmission ratio distortion in backcross hybrid genomes, providing further insight into the genomic architecture of genetic incompatibilities. Notably, regions with high levels of genetic divergence between species were enriched for genes associated with developmental and meiotic processes, providing strong candidates for postzygotic isolating barriers. These findings mark significant contributions to our understanding of the genetic basis of reproductive isolation between species undergoing character displacement. Furthermore, the genomic resources presented here will be instrumental for studying speciation in darters, the most diverse vertebrate group in North America.

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BACKGROUND: The process by which populations evolve to become new species involves the emergence of various reproductive isolating barriers (RIB). Despite major advancements in understanding this complex process, very little is known about the order in which RIBs evolve or their relative contribution to the total restriction of gene flow during various stages of speciation. This is mainly due to the difficulties of studying reproductive isolation during the early stages of species formation. This study examines ecological and non-ecological RIB within and between Daphnia pulex and Daphnia pulicaria, two recently diverged species that inhabit distinct habitats and exhibit an unusual level of intraspecific genetic subdivision. RESULTS: We find that while ecological prezygotic barriers are close to completion, none of the non-ecological barriers can restrict gene flow between D. pulex and D. pulicaria completely when acting alone. Surprisingly, we also identified high levels of postzygotic reproductive isolation in 'conspecific' interpopulation crosses of D. pulex. CONCLUSIONS: While the ecological prezygotic barriers are prevalent during the mature stages of speciation, non-ecological barriers likely dominated the early stages of speciation. This finding indicates the importance of studying the very early stages of speciation and suggests the contribution of postzygotic isolation in initiating the process of speciation.

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Neotropical cichlid fishes are one of the most diversified and evolutionarily successful species assemblages. Extremely similar forms and intraspecific polychromatism present challenges for the taxonomy of some of these groups. Several species complexes have a largely unknown origin and unresolved evolutionary processes. Dwarf cichlids of the genus Apistogramma, comprising more than a hundred species, exhibit intricate taxonomic and biogeographic patterns, with both allopatric and sympatric distributions. However, karyotype evolution and the role of chromosomal changes in Apistogramma are still unknown. In the present study, nine South American Apistogramma species were analyzed using conventional cytogenetic methods and the mapping of repetitive DNA sequences [18S rDNA, 5S rDNA, and (TTAGGG)n] by fluorescence in situ hybridization (FISH). Our results showed that Apistogramma has unique cytogenetic characteristics in relation to closely related groups, such as a reduced 2n and a large number of bi-armed chromosomes. Interspecific patterns revealed a scenario of remarkable karyotypic changes, including a reduction of 2n, the occurrence of B-chromosomes and evolutionary dynamic of rDNA tandem repeats. In addition to the well-known pre-zygotic reproductive isolation, the karyotype reorganization in the genus suggests that chromosomal changes could act as postzygotic barriers in areas where Apistogramma congeners overlap.

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Quantifying the relative contribution of multiple isolation barriers to gene flow between recently diverged species is essential for understanding speciation processes. In parapatric populations, local adaptation is thought to be a major contributor to the evolution of reproductive isolation. However, extrinsic postzygotic barriers assessed in reciprocal transplant experiments are often neglected in empirical assessments of multiple isolation barriers. We analyzed multiple isolation barriers between two closely related species of the plant genus Dianthus, a genus characterized by the most rapid species diversification in plants reported so far. Although D. carthusianorum L. and D. sylvestris Wulf. can easily be hybridized in crossing experiments, natural hybrids are rare. We found that in parapatry, pollinator-mediated prezygotic reproductive isolation barriers are important for both D. carthusianorum (0.761) and D. sylvestris (0.468). In contrast to D. carthusianorum, high hybrid viability in D. sylvestris (-0.491) was counteracted by strong extrinsic postzygotic isolation (0.900). Our study highlights the importance of including reciprocal transplant experiments for documenting extrinsic postzygotic isolation and demonstrates clearly divergent strategies and hence asymmetric pre- and postzygotic reproductive isolation between closely related species. It also suggests that pollinator-mediated and ecological isolation could have interacted in synergistic ways, further stimulating rapid speciation in Dianthus.

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Phylogenetic clades based on DNA sequences such as the chloroplast rbcL gene and the nuclear ITS region are frequently used to delimit algal species. However, these molecular markers cannot accurately delimit boundaries among some Ulva species. Although Ulva reticulata and Ulva ohnoi occasionally bloom in tropical to warm-temperate regions and are clearly distinguishable by their reticulate or plain blade morphology, they have few or no sequence divergences in these molecular markers and form a monophyletic clade. In this study, to clarify the speciation and species delimitation in the U. reticulata-ohnoi complex clade, reproductive relationships among several sexual strains from the Philippines and Japan including offspring that originated from the type specimen of U. ohnoi were examined by culturing and hybridization in addition to the ITS-based analysis. As a result, both prezygotic and postzygotic reproductive isolation were revealed to occur between genetically perforated U. reticulata and imperforate U. ohnoi. They were also separated on the basis of sequence analysis of the ITS region. That strongly supports that the two taxa are independent biological species. Although no prezygotic barrier among the Philippine and Japanese strains of U. reticulata was observed, unexpectedly zoospores produced by hybrid sporophytes in some of their combinations mostly failed to develop, indicating partial formation of a postzygotic barrier despite a 0.2% divergence in the ITS sequence. These findings suggest speciation is still ongoing in U. reticulata.

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