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Premise: Allopolyploidy-a hybridization-induced whole-genome duplication event-has been a major driver of plant diversification. The extent to which chromosomes pair with their proper homolog vs. with their homoeolog in allopolyploids varies across taxa, and methods to detect homoeologous gene flow (HGF) are needed to understand how HGF has shaped polyploid lineages. Methods: The ABBA-BABA test represents a classic method for detecting introgression between closely related species, but here we developed a modified use of the ABBA-BABA test to characterize the extent and direction of HGF in allotetraploid Coffea arabica. Results: We found that HGF is abundant in the C. arabica genome, with both subgenomes serving as donors and recipients of variation. We also found that HGF is highly maternally biased in plastid-targeted-but not mitochondrial-targeted-genes, as would be expected if plastid-nuclear incompatibilities exist between the two parent species. Discussion: Together, our analyses provide a simple framework for detecting HGF and new evidence consistent with selection favoring overwriting of paternally derived alleles by maternally derived alleles to ameliorate plastid-nuclear incompatibilities. Natural selection therefore appears to shape the direction and intensity of HGF in allopolyploid coffee, indicating that cytoplasmic inheritance has long-term consequences for polyploid lineages.

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The extent of interspecific gene flow and its consequences for the initiation, maintenance, and breakdown of species barriers in natural systems remain poorly understood. Interspecific gene flow by hybridization may weaken adaptive divergence, but can be overcome by selection against hybrids, which may ultimately promote reinforcement. An informative step towards understanding the role of gene flow during speciation is to describe patterns of past gene flow among extant species. We investigate signals of admixture between allopatric and sympatric populations of the two closely related European dung fly species Sepsis cynipsea and S. neocynipsea (Diptera: Sepsidae). Based on microsatellite genotypes, we first inferred a baseline demographic history using Approximate Bayesian Computation. We then used genomic data from pooled DNA of natural and laboratory populations to test for past interspecific gene flow based on allelic configurations discordant with the inferred population tree (ABBA-BABA test with D-statistic). Comparing the detected signals of gene flow with the contemporary geographic relationship among interspecific pairs of populations (sympatric vs. allopatric), we made two contrasting observations. At one site in the French Cevennes, we detected an excess of past interspecific gene flow, while at two sites in Switzerland we observed lower signals of past microsatellite genotypes gene flow among populations in sympatry compared to allopatric populations. These results suggest that the species boundaries between these two species depend on the past and/or present eco-geographic context in Europe, which indicates that there is no uniform link between contemporary geographic proximity and past interspecific gene flow in natural populations. Supplementary Information: The online version contains supplementary material available at 10.1007/s11692-023-09612-5.

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The evolutionary implications and frequency of hybridization and introgression are increasingly being recognized across the tree of life. To detect hybridization from multi-locus and genome-wide sequence data, a popular class of methods are based on summary statistics from subsets of 3 or 4 taxa. However, these methods often carry the assumption of a constant substitution rate across lineages and genes, which is commonly violated in many groups. In this work, we quantify the effects of rate variation on the D test (also known as ABBA-BABA test), the D3 test, and HyDe. All 3 tests are used widely across a range of taxonomic groups, in part because they are very fast to compute. We consider rate variation across species lineages, across genes, their lineage-by-gene interaction, and rate variation across gene-tree edges. We simulated species networks according to a birth-death-hybridization process, so as to capture a range of realistic species phylogenies. For all 3 methods tested, we found a marked increase in the false discovery of reticulation (type-1 error rate) when there is rate variation across species lineages. The D3 test was the most sensitive, with around 80% type-1 error, such that D3 appears to more sensitive to a departure from the clock than to the presence of reticulation. For all 3 tests, the power to detect hybridization events decreased as the number of hybridization events increased, indicating that multiple hybridization events can obscure one another if they occur within a small subset of taxa. Our study highlights the need to consider rate variation when using site-based summary statistics, and points to the advantages of methods that do not require assumptions on evolutionary rates across lineages or across genes.

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To understand how species evolve and adapt to changing environments, it is important to study gene flow and introgression due to their influence on speciation and radiation events. Here, we apply a novel experimental system for investigating these mechanisms using natural populations. The system is based on two fungal sister species with morphological and ecological similarities occurring in overlapping habitats. We examined introgression between these species by conducting whole genome sequencing of individuals from populations in North America and Europe. We assessed genome-wide nucleotide divergence and performed crossing experiments to study reproductive barriers. We further used ABBA-BABA statistics together with a network analysis to investigate introgression, and conducted demographic modelling to gain insight into divergence times and introgression events. The results revealed that the species are highly divergent and incompatible in vitro. Despite this, small regions of introgression were scattered throughout the genomes and one introgression event likely involves a ghost population (extant or extinct). This study demonstrates that introgression can be found among divergent species and that population histories can be studied without collections of all the populations involved. Moreover, the experimental system is shown to be a useful tool for research on reproductive isolation in natural populations.

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The human management of honey bees (Apis mellifera) has resulted in the widespread introduction of subspecies outside of their native ranges. One well known example of this is Apis mellifera mellifera, native to Northern Europe, which has now been significantly introgressed by the introduction of C lineage honey bees. Introgression has consequences for species in terms of future adaptive potential and long-term viability. However, estimating introgression in colony-living haplodiploid species is challenging. Previous studies have estimated introgression using individual workers, individual drones, multiple drones, and pooled workers. Here, we compare introgression estimates via three genetic approaches: SNP array, individual RAD-seq, and pooled colony RAD-seq. We also compare two statistical approaches: a maximum likelihood cluster program (ADMIXTURE) and an incomplete lineage sorting model (ABBA BABA). Overall, individual approaches resulted in lower introgression estimates than pooled colonies when using ADMIXTURE. However, the pooled colony ABBA BABA approach resulted in generally lower introgression estimates than all three ADMIXTURE estimates. These results highlight that sometimes one individual is not enough to assess colony-level introgression, and future studies that do use colony pools should not be solely dependent on clustering programs for introgression estimates.

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PREMISE: Oceanic islands offer the opportunity to understand evolutionary processes underlying rapid diversification. Along with geographic isolation and ecological shifts, a growing body of genomic evidence has suggested that hybridization can play an important role in island evolution. Here we use genotyping-by-sequencing (GBS) to understand the roles of hybridization, ecology, and geographic isolation in the radiation of Canary Island Descurainia (Brassicaceae). METHODS: We carried out GBS for multiple individuals of all Canary Island species and two outgroups. Phylogenetic analyses of the GBS data were performed using both supermatrix and gene tree approaches and hybridization events were examined using D-statistics and Approximate Bayesian Computation. Climatic data were analyzed to examine the relationship between ecology and diversification. RESULTS: Analysis of the supermatrix data set resulted in a fully resolved phylogeny. Species networks suggest a hybridization event has occurred for D. gilva, with these results being supported by Approximate Bayesian Computation analysis. Strong phylogenetic signals for temperature and precipitation indicate one major ecological shift within Canary Island Descurainia. CONCLUSIONS: Inter-island dispersal played a significant role in the diversification of Descurainia, with evidence of only one major shift in climate preferences. Despite weak reproductive barriers and the occurrence of hybrids, hybridization appears to have played only a limited role in the diversification of the group with a single instance detected. The results highlight the need to use phylogenetic network approaches that can simultaneously accommodate incomplete lineage sorting and gene flow when studying groups prone to hybridization; patterns that might otherwise be obscured in species trees.

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Incomplete lineage sorting (ILS) and introgression have been increasingly recognized as important processes involved in biological differentiation. Both ILS and introgression result in incongruences between gene trees and species trees, consequently causing difficulties in phylogenetic reconstruction. This is particularly the case for rapid radiations, as short internodal distances and incomplete reproductive isolation increase the likelihood of both ILS and introgression. Estimation of the relative frequency of these processes requires assessments across many genomic regions. We use transcriptomics to test for introgression and estimate the frequency of ILS in a set of three closely related and geographically adjacent South American tuco-tucos species (Ctenomys), a genus comprising 64 species resulting from recent, rapid radiation. After cleaning and filtering, 5764 orthologous genes strongly support paraphyly of C. pearsoni relative to C. brasiliensis (putatively represented by the population of Villa Serrana). In line with earlier phylogenetic work, the C. pearsoni - C. brasiliensis pair is closely related to C. torquatus, whereas C. rionegrensis is more distantly related to these three nominal species. Classical Patterson's d-statistic shows significant signals of introgression from C. torquatus into C. brasiliensis. However, a 5-taxon test shows no significant results. ILS was estimated to have involved about 9% of the loci, suggesting it represents an important process in the incipient diversification of tuco-tucos.

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The detection of introgression from genomic data is transforming our view of species and the origins of adaptive variation. Among the most widely used approaches to detect introgression is the so-called ABBA-BABA test or D-statistic, which identifies excess allele sharing between nonsister taxa. Part of the appeal of D is its simplicity, but this also limits its informativeness, particularly about the timing and direction of introgression. Here we present a simple extension, D frequency spectrum or DFS, in which D is partitioned according to the frequencies of derived alleles. We use simulations over a large parameter space to show how DFS carries information about various factors. In particular, recent introgression reliably leads to a peak in DFS among low-frequency derived alleles, whereas violation of model assumptions can lead to a lack of signal at low frequencies. We also reanalyze published empirical data from six different animal and plant taxa, and interpret the results in the light of our simulations, showing how DFS provides novel insights. We currently see DFS as a descriptive tool that will augment both simple and sophisticated tests for introgression, but in the future it may be usefully incorporated into probabilistic inference frameworks.

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Patterson's D, also known as the ABBA-BABA statistic, and related statistics such as the f4 -ratio, are commonly used to assess evidence of gene flow between populations or closely related species. Currently available implementations often require custom file formats, implement only small subsets of the available statistics, and are impractical to evaluate all gene flow hypotheses across data sets with many populations or species due to computational inefficiencies. Here, we present a new software package Dsuite, an efficient implementation allowing genome scale calculations of the D and f4 -ratio statistics across all combinations of tens or hundreds of populations or species directly from a variant call format (VCF) file. Our program also implements statistics suited for application to genomic windows, providing evidence of whether introgression is confined to specific loci, and it can also aid in interpretation of a system of f4 -ratio results with the use of the "f-branch" method. Dsuite is available at https://github.com/millanek/Dsuite, is straightforward to use, substantially more computationally efficient than comparable programs, and provides a convenient suite of tools and statistics, including some not previously available in any software package. Thus, Dsuite facilitates the assessment of evidence for gene flow, especially across larger genomic data sets.

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Many methods exist for detecting introgression between nonsister species, but the most commonly used require either a single sequence from four or more taxa or multiple sequences from each of three taxa. Here, we present a test for introgression that uses only a single sequence from three taxa. This test, denoted D3, uses similar logic as the standard D-test for introgression, but by using pairwise distances instead of site patterns it is able to detect the same signal of introgression with fewer species. We use simulations to show that D3 has statistical power almost equal to D, demonstrating its use on a data set of wild bananas (Musa). The new test is easy to apply and easy to interpret, and should find wide use among currently available data sets.

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BACKGROUND: Coalescent-based species tree inference has become widely used in the analysis of genome-scale multilocus and SNP datasets when the goal is inference of a species-level phylogeny. However, numerous evolutionary processes are known to violate the assumptions of a coalescence-only model and complicate inference of the species tree. One such process is hybrid speciation, in which a species shares its ancestry with two distinct species. Although many methods have been proposed to detect hybrid speciation, only a few have considered both hybridization and coalescence in a unified framework, and these are generally limited to the setting in which putative hybrid species must be identified in advance. RESULTS: Here we propose a method that can examine genome-scale data for a large number of taxa and detect those taxa that may have arisen via hybridization, as well as their potential "parental" taxa. The method is based on a model that considers both coalescence and hybridization together, and uses phylogenetic invariants to construct a test that scales well in terms of computational time for both the number of taxa and the amount of sequence data. We test the method using simulated data for up 20 taxa and 100,000bp, and find that the method accurately identifies both recent and ancient hybrid species in less than 30 s. We apply the method to two empirical datasets, one composed of Sistrurus rattlesnakes for which hybrid speciation is not supported by previous work, and one consisting of several species of Heliconius butterflies for which some evidence of hybrid speciation has been previously found. CONCLUSIONS: The proposed method is powerful for detecting hybridization for both recent and ancient hybridization events. The computations required can be carried out rapidly for a large number of sequences using genome-scale data, and the method is appropriate for both SNP and multilocus data.

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Introgression is a pervasive biological process, and many statistical methods have been developed to infer its presence from genomic data. However, many of the consequences and genomic signatures of introgression remain unexplored from a methodological standpoint. Here, we develop a model for the timing and direction of introgression based on the multispecies network coalescent, and from it suggest new approaches for testing introgression hypotheses. We suggest two new statistics, D1 and D2, which can be used in conjunction with other information to test hypotheses relating to the timing and direction of introgression, respectively. D1 may find use in evaluating cases of homoploid hybrid speciation (HHS), while D2 provides a four-taxon test for polarizing introgression. Although analytical expectations for our statistics require a number of assumptions to be met, we show how simulations can be used to test hypotheses about introgression when these assumptions are violated. We apply the D1 statistic to genomic data from the wild yeast Saccharomyces paradoxus-a proposed example of HHS-demonstrating its use as a test of this model. These methods provide new and powerful ways to address questions relating to the timing and direction of introgression.

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Introgression is now commonly reported in studies across the Tree of Life, aided by recent advancements in data collection and analysis. Nevertheless, researchers working with nonmodel species lacking reference genomes may be stymied by a mismatch between available resources and methodological demands. In this study, we demonstrate a fast and simple approach for inferring introgression using RADseq data, and apply it to a case study involving spiny lizards (Sceloporus) from northeastern México. First, we find evidence for recurrent mtDNA introgression between the two focal species based on patterns of mito-nuclear discordance. We then test for nuclear introgression by exhaustively applying the "five-taxon" D-statistic (DFOIL ) to all relevant individuals sampled for RADseq data. In our case, this exhaustive approach (dubbed "ExDFOIL ") entails testing up to ~250,000 unique four-taxon combinations of individuals across species. To facilitate use of this ExDFOIL approach, we provide scripts for many relevant tasks, including the selection of appropriate four-taxon combinations, execution of DFOIL tests in parallel and visualization of introgression results in phylogenetic and geographic space. Using ExDFOIL , we find evidence for ancient introgression between the focal species. Furthermore, we reveal geographic variation in patterns of introgression that is consistent with patterns of mito-nuclear discordance and with recurrent introgression. Overall, our study demonstrates that the combination of DFOIL and RADseq data can effectively detect introgression under a variety of sampling conditions (for individuals, populations and loci). Importantly, we also find evidence that batch-specific error and linkage in RADseq data may mislead inferences of introgression under certain conditions.

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The detection of ancient gene flow between human populations is an important issue in population genetics. A common tool for detecting ancient admixture events is the D-statistic. The D-statistic is based on the hypothesis of a genetic relationship that involves four populations, whose correctness is assessed by evaluating specific coincidences of alleles between the groups. When working with high-throughput sequencing data, calling genotypes accurately is not always possible; therefore, the D-statistic currently samples a single base from the reads of one individual per population. This implies ignoring much of the information in the data, an issue especially striking in the case of ancient genomes. We provide a significant improvement to overcome the problems of the D-statistic by considering all reads from multiple individuals in each population. We also apply type-specific error correction to combat the problems of sequencing errors, and show a way to correct for introgression from an external population that is not part of the supposed genetic relationship, and how this leads to an estimate of the admixture rate. We prove that the D-statistic is approximated by a standard normal distribution. Furthermore, we show that our method outperforms the traditional D-statistic in detecting admixtures. The power gain is most pronounced for low and medium sequencing depth (1-10×), and performances are as good as with perfectly called genotypes at a sequencing depth of 2×. We show the reliability of error correction in scenarios with simulated errors and ancient data, and correct for introgression in known scenarios to estimate the admixture rates.

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PREMISE: Wild sunflowers harbor considerable genetic diversity and are a major resource for improvement of the cultivated sunflower, Helianthus annuus. The Helianthus genus is also well known for its propensity for gene flow between taxa. METHODS: We surveyed genomic diversity of 292 samples of wild Helianthus from 22 taxa that are cross-compatible with the cultivar using genotyping by sequencing. With these data, we derived a high-resolution phylogeny of the taxa, interrogated genome-wide levels of diversity, explored H. annuus population structure, and identified localized gene flow between H. annuus and its close relatives. KEY RESULTS: Our phylogenomic analyses confirmed a number of previously established interspecific relationships and indicated for the first time that a newly described annual sunflower, H. winteri, is nested within H. annuus. Principal component analyses showed that H. annuus has geographic population structure with most notable subpopulations occurring in California and Texas. While gene flow was identified between H. annuus and H. bolanderi in California and between H. annuus and H. argophyllus in Texas, this genetic exchange does not appear to drive observed patterns of H. annuus population structure. CONCLUSIONS: Wild H. annuus remains an excellent resource for cultivated sunflower breeding effort because of its diversity and the ease with which it can be crossed with cultivated H. annuus. Cases of interspecific gene flow such as those documented here also indicate wild H. annuus can act as a bridge to capture alleles from other wild taxa; continued breeding efforts with it may therefore reap the largest rewards.

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The Devils Hole pupfish (Cyprinodon diabolis; DHP) is an icon of conservation biology. Isolated in a 50 m(2) pool (Devils Hole), DHP is one of the rarest vertebrate species known and an evolutionary anomaly, having survived in complete isolation for thousands of years. However, recent findings suggest DHP might be younger than commonly thought, potentially introduced to Devils Hole by humans in the past thousand years. As a result, the significance of DHP from an evolutionary and conservation perspective has been questioned. Here we present a high-resolution genomic analysis of DHP and two closely related species, with the goal of thoroughly examining the temporal divergence of DHP. To this end, we inferred the evolutionary history of DHP from multiple random genomic subsets and evaluated four historical scenarios using the multispecies coalescent. Our results provide substantial information regarding the evolutionary history of DHP. Genomic patterns of secondary contact present strong evidence that DHP were isolated in Devils Hole prior to 20-10 ka and the model best supported by geological history and known mutation rates predicts DHP diverged around 60 ka, approximately the same time Devils Hole opened to the surface. We make the novel prediction that DHP colonized and have survived in Devils Hole since the cavern opened, and the two events (colonization and collapse of the cavern's roof) were caused by a common geologic event. Our results emphasize the power of evolutionary theory as a predictive framework and reaffirm DHP as an important evolutionary novelty, worthy of continued conservation and exploration.

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When multiple speciation events occur rapidly in succession, discordant genealogies due to incomplete lineage sorting (ILS) can complicate the detection of introgression. A variety of methods, including the [Formula: see text]-statistic (a.k.a. the "ABBA-BABA test"), have been proposed to infer introgression in the presence of ILS for a four-taxon clade. However, no integrated method exists to detect introgression using allelic patterns for more complex phylogenies. Here we explore the issues associated with previous systems of applying [Formula: see text]-statistics to a larger tree topology, and propose new [Formula: see text] tests as an integrated framework to infer both the taxa involved in and the direction of introgression for a symmetric five-taxon phylogeny. Using theory and simulations, we show that the [Formula: see text] statistics correctly identify the introgression donor and recipient lineages, even at low rates of introgression. [Formula: see text] is also shown to have extremely low false-positive rates. The [Formula: see text] tests are computationally inexpensive to calculate and can easily be applied to phylogenomic data sets, both genome-wide and in windows of the genome. In addition, we explore both the principles and problems of introgression detection in even more complex phylogenies.

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Several methods have been proposed to test for introgression across genomes. One method tests for a genome-wide excess of shared derived alleles between taxa using Patterson's D statistic, but does not establish which loci show such an excess or whether the excess is due to introgression or ancestral population structure. Several recent studies have extended the use of D by applying the statistic to small genomic regions, rather than genome-wide. Here, we use simulations and whole-genome data from Heliconius butterflies to investigate the behavior of D in small genomic regions. We find that D is unreliable in this situation as it gives inflated values when effective population size is low, causing D outliers to cluster in genomic regions of reduced diversity. As an alternative, we propose a related statistic ƒ(d), a modified version of a statistic originally developed to estimate the genome-wide fraction of admixture. ƒ(d) is not subject to the same biases as D, and is better at identifying introgressed loci. Finally, we show that both D and ƒ(d) outliers tend to cluster in regions of low absolute divergence (d(XY)), which can confound a recently proposed test for differentiating introgression from shared ancestral variation at individual loci.

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Young species complexes that are widespread across ecologically disparate regions offer important insights into the process of speciation because of their relevance to how local adaptation and gene flow influence diversification. We used mitochondrial DNA and up to 28 152 genomewide single nucleotide polymorphisms from polytypic barking frogs (Craugastor augusti complex) to infer phylogenetic relationships and test for the signature of introgressive hybridization among diverging lineages. Our phylogenetic reconstructions suggest (i) a rapid Pliocene-Pleistocene radiation that produced at least nine distinct lineages and (ii) that geographic features of the arid Central Mexican Plateau contributed to two independent northward expansions. Despite clear lineage differentiation (many private alleles and high between-lineage FST scores), D-statistic tests, which differentiate introgression from ancestral polymorphism, allowed us to identify two putative instances of reticulate gene flow. Partitioned D-statistics provided evidence that these events occurred in the same direction between clades but at different points in time. After correcting for geographic distance, we found that lineages involved in hybrid gene flow interactions had higher levels of genetic variation than independently evolving lineages. These findings suggest that the nature of hybrid compatibility can be conserved overlong periods of evolutionary time and that hybridization between diverging lineages may contribute to standing levels of genetic variation.

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