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Recent genomic analyses have highlighted the prevalence of speciation with gene flow in many taxa and have underscored the importance of accounting for these reticulate evolutionary processes when constructing species trees and generating parameter estimates. This is especially important for deepening our understanding of speciation in the sea where fast moving ocean currents, expanses of deep water, and periodic episodes of sea level rise and fall act as soft and temporary allopatric barriers that facilitate both divergence and secondary contact. Under these conditions, gene flow is not expected to cease completely while contemporary distributions are expected to differ from historical ones. Here we conduct range-wide sampling for Pederson’s cleaner shrimp (Ancylomenes pedersoni), a species complex from the Greater Caribbean that contains three clearly delimited mitochondrial lineages with both allopatric and sympatric distributions. Using mtDNA barcodes and a genomic ddRADseq approach, we combine classic phylogenetic analyses with extensive topology testing and demographic modeling (10 site frequency replicates x 45 evolutionary models x 50 model simulations/replicate = 22,500 simulations) to test species boundaries and reconstruct the evolutionary history of what was expected to be a simple case study. Instead, our results indicate a history of allopatric divergence, secondary contact, introgression, and endemic hybrid speciation driven by the final closure of the Isthmus of Panama and the strengthening of the Gulf Stream Current ~3.5 million years ago. The history of this species complex recovered by model-based methods that allow reticulation differs from that recovered by standard phylogenetic analyses and is unexpected given contemporary distributions. The geologically and biologically meaningful insights gained by our model selection analyses illuminate a novel pathway of species formation that resulted from one of the most biogeographically significant events in Earth’s history.

How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, implying that speciation is a series of splits between lineages. Yet gene flow between good species is increasingly recognized as an important mechanism in the diversification of radiations, often spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied in cases involving few species, or geographically restricted to spaces like islands, but not on the scale of a continental radiation. Previous studies have documented gene flow, adaptive introgression and hybrid speciation in a small subsection of the charismatic Neotropical butterflies Heliconius. Using genome-wide resequencing of 40 out of 45 species in the genus we demonstrate for the first time that admixture has played a role throughout the evolution of Heliconius and the sister genus Eueides. Modelling of phylogenetic networks based on 6848 orthologous autosomal genes (Maximum Pseudo-Likelihood Networks) or 5,483,419 high quality SNPs (Ancestral Recombination Graph) uncovers nine new cases of interspecific gene flow at up to half of the genome. However, f4 statistics of admixture show that the extent of the process has varied between subgenera. Evidence for introgression is found at all five loci controlling the colour and shape of the mimetic wing patterns, including in the putative hybrid species H. hecalesia, characterised by an unusual hindwing. Due to hybridization and incomplete coalescence during rapid speciation, individual gene trees show rampant discordance. Although reduced gene flow and faster coalescence are expected at the Z chromosome, we discover high levels of conflict between the 416 sex-linked loci. Despite this discordant pattern, both concatenation and multispecies coalescent approaches yield surprisingly consistent and fully supported genome-wide phylogenies. We conclude that the imposition of the bifurcating tree model without testing for interspecific gene flow may distort our perception of adaptive radiations and thus the ability to study trait evolution in a comparative framework.

The origin and dispersal of cultivated and wild mandarin and related citrus are poorly understood. Here, comparative genome analysis of 69 new east Asian genomes and other mainland Asian citrus reveals a previously unrecognized wild sexual species native to the Ryukyu Islands: C. ryukyuensis sp. nov. The taxonomic complexity of east Asian mandarins then collapses to a satisfying simplicity, accounting for tachibana, shiikuwasha, and other traditional Ryukyuan mandarin types as homoploid hybrid species formed by combining C. ryukyuensis with various mainland mandarins. These hybrid species reproduce clonally by apomictic seed, a trait shared with oranges, grapefruits, lemons and many cultivated mandarins. We trace the origin of apomixis alleles in citrus to mangshanyeju wild mandarins, which played a central role in citrus domestication via adaptive wild introgression. Our results provide a coherent biogeographic framework for understanding the diversity and domestication of mandarin-type citrus through speciation, admixture, and rapid diffusion of apomictic reproduction., To explore the nature of wild and cultivated mandarins, the authors carry out genomic analysis of diverse east Asian citrus. The discovery of a wild species Citrus ryukyuensis native to the Ryukyu islands and a new population of wild mainland Asian mandarin explains the origin and diversity of mandarins and their ability to reproduce apomictically.

We studied hybrid interactions ofLilium meleagrinum,Lilium gongshanense, andLilium saluenenseusing an integrative approach combining population genetics, fieldwork, and phenological research. These three species occur along an elevational gradient, withL. meleagrinumoccurring at lower elevations,L. saluenenseat higher elevations, andL. gongshanensebetween them. The species show strong morphological differentiation despite there being no clear environmental barriers to gene flow among them.Lilium gongshanenseis likely to have a hybrid origin based on our prior work, but its progenitors remain uncertain. We sought to determine whether gene flow occurs among these three parapatric species, and, if so, whetherL. gongshanenseis a hybrid ofL. meleagrinumand/orL. saluenense. We analyzed data from multiple chloroplast genes and spacers, nuclear internal transcribed spacer (ITS), and 18 nuclear Expressed Sequence Tag-Simple Sequence Repeat (EST-SSR) microsatellites for accessions of the three species representing dense population-level sampling. We also inferred phenology by examining species in the field and using herbarium specimens. We found that there are only two types of chloroplast genomes shared among the three species and thatL. gongshanenseforms two distinct groups with closest links to other species ofLiliumbased on ITS. Taken together,L. gongshanenseis unlikely to be a hybrid species resulting from a cross betweenL. meleagrinumandL. saluenense, but gene flow is occurring among the three species. The gene flow is likely to be rare according to evidence from all molecular datasets, and this is corroborated by detection of only one putative hybrid individual in the field and asynchronous phenology. We suspect that the rarity of hybridization events among the species facilitates their continued genetic separation.

In this chapter is analyzed one characteristic of the reproductive behavior that is frequently found among crocodilian species: hybridization. Hybridization is defined as reproduction between members of genetically distinct populations, producing offspring of mixed ancestry. The phenomenon of hybridization and hybrid speciation has been a topic of extensive discussion because it questions the concept of biological species. These discussions include topics such as sexual compatibility between species, fertility or not of hybrid offspring, phenotypic or genotypic similarity of hybrids, hybrid vigor, and potential hybrid zones. Crocodiles are long-lived and ancient species, but their specimens are very promiscuous and sexually actives in their reproduction seasons. In this context, hybridization was and is a significant force in evolution to crocodilians. In this chapter, the different mechanisms that influence hybridization processes, the effects of hybridization at different evolutionary levels, species boundaries in hybrid zones, methodologies for the study of this phenomenon, main results of hybridization studies, and the conservation status of parental and hybrid species in New-World crocodile species are discussed.

Repeated homoploid hybrid speciation (HHS) events with the same parental species have rarely been reported. In this study, we used population transcriptome data to test paraphyly and HHS events in one conifer Picea brachytyla. All analyses identified and supported non-sister relationships for the two lineages of P. brachytyla. The southern lineage was placed within the re-circumscribed P. likiangensis species complex (PLSC) while P. brachytyla sensu stricto (s.s.), comprising only the northern lineage, parallels both PLSC and the closely related P. wilsonii. In addition, both phylogenetic and coalescent analyses suggested that P. brachytyla s.s. arose from homoploid hybrid speciation between the ancestor of the PLSC before its diversification (into the current varieties or species), and P. wilsonii, through an intermediate hybrid lineage at an early stage and backcrossing to the ancestral PLSC. These two parental ancestors also produced another homoploid hybrid species, P. purpurea, in the same way but at a later stage, through the same extinct lineage but backcrossing to the other parent, P. wilsonii. We reveal the first case that backcrossing to different parents of the same extinct hybrid lineage produced two different hybrid species. Our results highlight the existence of more reticulate evolution during species diversification in the spruce genus and more complex homoploid hybrid events than have previously been identified.

Hybridization and polyploidization are powerful mechanisms of speciation. Hybrid speciation often coincides with whole-genome duplication (WGD) in eukaryotes. This suggests that WGD allows hybrids to thrive by restoring fertility and/or increasing access to adaptive mutations. Alternatively, it has been suggested that hybridization itself may trigger WGD. Testing these models requires quantifying the rate of WGD in hybrids without the confounding effect of natural selection. By measuring the spontaneous rate of WGD of 1304 yeast crosses evolved under relaxed selection, we show that some genotypes are more prone to WGD and WGD can be triggered by hybridization. We also find that higher WGD rate correlates with higher genomic instability and that WGD increases fertility and genetic variability. These results provide evidence that hybridization itself can promote WGD, which in turn facilitates the evolution of hybrids.

Insight into complex evolutionary histories continues to build through broad comparative phylogenomic and population genomic studies. In particular, there is a need to understand the extent and scale that gene flow contributes to standing genomic diversity and the role introgression has played in evolutionary processes such as hybrid speciation. Here, we investigate the evolutionary history of the Mergini tribe (sea ducks) by coupling multi-species comparisons with phylogenomic analyses of thousands of nuclear ddRAD-seq loci, including Z-sex chromosome and autosomal linked loci, and the mitogenome assayed across all extant sea duck species in North America. All sea duck species are strongly structured across all sampled marker types (pair-wise species ΦST > 0.2), with clear genetic assignments of individuals to their respective species, and phylogenetic relationships recapitulate known relationships. Despite strong species integrity, we identify at least 18 putative hybrids; with all but one being late generational backcrosses. Most interesting, we provide the first evidence that an ancestral gene flow event between long-tailed ducks (Clangula hyemalis) and true Eiders (Somateria spp.) not only moved genetic material into the former species, but likely generated a novel species — the Steller’s eider (Polysticta stelleri) — via hybrid speciation. Despite generally low contemporary levels of gene flow, we conclude that hybridization has and continues to be an important process that shifts novel genetic variation between species within the tribe Mergini. Finally, we outline methods that permit researchers to contrast genomic patterns of contemporary versus ancestral gene flow when attempting to reconstruct potentially complex evolutionary histories.

Heterozygotes for major chromosomal rearrangements such as fusions and fissions are expected to display a high level of sterility due to problems during meiosis. However, some species, especially plants and animals with holocentric chromosomes, are known to tolerate chromosomal heterozygosity even for multiple rearrangements. Here, we studied male meiotic chromosome behavior in four hybrid generations (F1–F4) between two chromosomal races of the Wood White butterfly Leptidea sinapis differentiated by at least 24 chromosomal fusions/fissions. Previous work showed that these hybrids were fertile, although their fertility was reduced as compared to crosses within chromosomal races. We demonstrate that (i) F1 hybrids are highly heterozygous with nearly all chromosomes participating in the formation of trivalents at the first meiotic division, and (ii) that from F1 to F4 the number of trivalents decreases and the number of bivalents increases. We argue that the observed process of chromosome sorting would, if continued, result in a new homozygous chromosomal race, i.e., in a new karyotype with intermediate chromosome number and, possibly, in a new incipient homoploid hybrid species. We also discuss the segregational model of karyotype evolution and the chromosomal model of homoploid hybrid speciation., Support for this research was provided by the Russian Science Foundation No. 19-14-00202 to VL, by the Academy of Finland to VD (decision no. 328895), by the Royal Swedish Academy of Sciences to MF, and by the Spanish AEI/FEDER, UE (CGL2016-76322-P and PID2019-107078GB-I00) to RV.

Allopolyploidization, which involves hybridization and genome doubling, is a key driving force in higher plant evolution. The transcriptome reprogramming that accompanies allopolyploidization can cause extensive phenotypic variations, and thus confers allopolyploids higher evolutionary potential than their diploid progenitors. Despite many studies, little is known about the interplay between hybridization and genome doubling in transcriptome reprogramming during allopolyploidization. Here, we performed genome-wide analyses of gene expression and splicing changes during allopolyploidization in wheat and brassica lineages. Our results indicated that both hybridization and genome doubling can induce genome-wide transcriptional and splicing changes. Notably, the gene transcriptional and splicing changes caused by hybridization can be largely recovered to parental levels by genome doubling in allopolyploids. Since transcriptome reprogramming is an important contributor to heterosis, our results revealed that only part of the heterosis in hybrids can be fixed in allopolyploids through genome doubling. Therefore, our findings update the current understanding of the permanent fixation of heterosis in hybrids through genome doubling. In addition, our results indicated that a large proportion of the transcriptome reprogramming in interspecific hybrids was not caused by the merging of two parental genomes, providing novel insights into the mechanism of heterosis.

Species in the genus Suaeda have few diagnostic characters and substantial morphological plasticity. Hence, regional floras do not provide clear taxonomic information for Suaeda spp. in East Asia. In order to assess the taxonomy of four species in the genus Suaeda (S. australis, S. maritima, S. japonica, and S. heteroptera), cpDNA (rpl32-trnL and trnH-psbA), nDNA (ITS), and MIG-seq analyses were carried out. Genome-wide SNP results indicated three lineages: (1) S. australis in Korea and S. maritima in Japan, (2) S. maritima in Korea and S. heteroptera in China, and (3) S. japionica. In phylogenetic trees and genotype analyses, cpDNA and nDNA results showed discrepancies, while S. japonica and S. maritima in Korea, and S. heteroptera in China shared the same haplotype and ribotype. We suggest that the shared haplotype may be due to chloroplast capture. Based on our results, we assume that S. japonica was formed by homoploid hybrid speciation between the two lineages.

It is increasingly realized that homoploid hybrid speciation (HHS), which involves no change in chromosome number, is an important mechanism of speciation. HHS will likely increase in frequency as ecological and geographical barriers between species are continuing to be disrupted by human activities. HHS requires the establishment of reproductive isolation between a hybrid and its parents, but the underlying genes and genetic mechanisms remain largely unknown. In this study, we reveal by integrated approaches that reproductive isolation originates in one homoploid hybrid plant species through the inheritance of alternate alleles at genes that determine parental premating isolation. The parent species of this hybrid species are reproductively isolated by differences in flowering time and survivorship on soils containing high concentrations of iron. We found that the hybrid species inherits alleles of parental isolating major genes related to flowering time from one parent and alleles of major genes related to iron tolerance from the other parent. In this way, it became reproductively isolated from one parent by the difference in flowering time and from the other by habitat adaptation (iron tolerance). These findings and further modeling results suggest that HHS may occur relatively easily via the inheritance of alternate parental premating isolating genes and barriers.

The Pannonian endemic species Vincetoxicum pannonicum was described from specimens collected in Hungary and occurs at only few locations. It is considered “vulnerable” according to the International Red List. The chromosome set was reported to be tetraploid, and the species was hypothesized to be an allotetraploid hybrid of the Balkan species V. fuscatum and the Adriatic species hirundinaria subsp. adriaticum. We investigated the origin of V. pannonicum using molecular phylogenetic methods by separately analyzing the multicopy nuclear ribosomal internal transcribed spacer (nrITS) and the plastid-encoded trnH-psbA DNA regions and by evaluating discrepancies between the produced gene trees. Paralogs in the nrITS region clustered in two main groups, one of which was closest to V. fuscatum, and the other included V. hirundinaria subsp. adriaticum. According to trnH-psbA sequences, V. pannonicum and V. hirundinaria subsp. adriaticum formed a single group. Our results show that V. pannonicum diversified because of hybrid speciation, in which V. fuscatum was the pollen donor. We discovered a similar placement of V. maeoticum, which suggests a further hybridization event between V. fuscatum and a species of the V. hirundinaria group. Our genome-size estimate indicates almost sixfold larger genome size in V. pannonicum compared to the maternal diploid parent, suggesting hexaploidy; however, V. pannonicum is tetraploid. This may suggest cytological diploidization in the allopolyploid V. pannonicum. We observed substantial genetic distance between V. hirundinaria subsp. adriaticum and all other subspecies of V. hirundinaria, and we therefore propose that V. adriaticum should be regarded as a separate species.

Hybridisation can lead to homoploid hybrid speciation, i.e., the origin of new species without change in chromosome number between parents and offspring. Central to homoploid hybrid speciation is the role of hybridisation in the establishment of reproductive isolation between the hybrid and the parental species in the early stages of speciation, when typically all species occur at least partly in sympatry. In this work we analyse genome-wide polymorphism data obtained by transcriptome sequencing of the British hybrid species Oxford ragwort (Senecio squalidus, Asteraceae), its two Italian parental species (S. aethnensis and S. chrysanthemifolius) and their naturally occurring hybrids on Mt Etna (Italy). We show that Oxford ragwort most likely originated from de novo hybridisation between its two Italian parental species whilst they were in cultivation in British gardens at the turn of the 18th century. Reproductive isolation between the new hybrid species and its parental species probably resulted from inheritance of genetic incompatibilities between the two parental species and subsequent ecological segregation - both of which have been shown in previous studies. Our results imply that S. squalidus meets the most stringent criteria set forth to identify homoploid hybrid speciation, and call attention to the creative role of hybridisation in responding to novel environmental conditions.

Hybridization can drive speciation. We examine the hypothesis that Castanea henryi var. omeiensis is an evolutionary lineage that originated from hybridization between two near-sympatric diploid taxa, C. henryi var. henryi and C. mollissima. We produce a high-quality genome assembly for mollissima and characterize evolutionary relationships among related chestnut taxa. Our results show that C. henryi var. omeiensis has a mosaic genome but has accumulated divergence in all 12 chromosomes. We observe positive correlation between admixture proportions and recombination rates across the genome. Candidate barrier genomic regions, which isolate var. henryi and mollissima, are re-assorted in the hybrid lineage. We further find that the putative barrier segments concentrate in genomic regions with less recombination, suggesting that interaction between natural selection and recombination shapes the evolution of hybrid genomes during hybrid speciation. This study highlights that reassortment of parental barriers is an important mechanism in generating biodiversity., Chinese chestnut is widely cultivated for nut production and harbors value as a genetic resource for restoration of American and European chestnut trees destroyed by chestnut blight. Here, the authors reveal the genomic basis of homoploid hybrid speciation within Castanea spp. and find the nonrandom distribution of reproductive barrier loci based on a high-quality reference genome.

Inferring the frequency and mode of hybridization among closely related organisms is an important step for understanding the process of speciation and can help to uncover reticulated patterns of phylogeny more generally. Phylogenomic methods to test for the presence of hybridization come in many varieties and typically operate by leveraging expected patterns of genealogical discordance in the absence of hybridization. An important assumption made by these tests is that the data (genes or SNPs) are independent given the species tree. However, when the data are closely linked, it is especially important to consider their non-independence. Recently, deep learning techniques such as convolutional neural networks (CNNs) have been used to perform population genetic inferences with linked SNPs coded as binary images. Here we use CNNs for selecting among candidate hybridization scenarios using the tree topology (((P1,P2),P3),Out) and a matrix of pairwise nucleotide divergence (dXY) calculated in windows across the genome. Using coalescent simulations to train and independently test a neural network showed that our method, HyDe-CNN, was able to accurately perform model selection for hybridization scenarios across a wide-breath of parameter space. We then used HyDe-CNN to test models of admixture inHeliconiusbutterflies, as well as comparing it to a random forest classifier trained on introgression-based statistics. Given the flexibility of our approach, the dropping cost of long-read sequencing, and the continued improvement of CNN architectures, we anticipate that inferences of hybridization using deep learning methods like ours will help researchers to better understand patterns of admixture in their study organisms.

Hybridization is well recognized as a driver of speciation, yet it often remains difficult to parse phylogenomically in that post-speciation gene flow frequently supersedes an ancestral signal. Here we examined how interactions between recombination and gene flow shaped the phylogenomic landscape of red wolf to create non-random retention of introgressed ancestry. Our re-analyses of genomic data recapitulate fossil evidence by demonstrating red wolf was indeed extant and isolated prior to more recent admixture with other North American canids. Its more ancient divergence, now sequestered within low-recombinant regions on the X-chromosome (i.e., chromosomal ‘refugia’), is effectively masked by multiple, successive waves of secondary introgression that now dominate its autosomal ancestry. These interpretations are congruent with more theoretical explanations that describe the manner by which introgression can be localized within the genome through recombination and selection. They also tacitly support the large-X effect, i.e., the manner by which loci that contribute to reproductive isolation can be enriched on the X-chromosome. By contrast, similar, high recombinant regions were also found as enriched within very shallow gene trees, thus reflecting post-speciation gene flow and a compression of divergence estimates to 1/20thof that found in recombination ‘cold spots’. Our results effectively reconcile conflicting hypotheses regarding the impact of hybridization on evolution of North American canids and support an emerging framework within which the analysis of a phylogenomic landscape structured by recombination can be used to successfully address the macroevolutionary implications of hybridization.

We also acknowledge the national funding bodies that have supported this work, including NERC, The Genetics Society, BBSRC and the Leverhulme Trust in the UK, NSF in the USA, and ARC in Australia. Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories and morphologies, and occupy a multitude of environments. Common within the genus are species that have hybridised naturally, undergone polyploidisation, and colonised diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology. Postprint

Congeneric parasites are unlikely to specialize on the same tissues of the same host species, likely because of strong multifarious selection against niche overlap. Exceptions where multiple congeneric species overlap on the same tissues may therefore reveal important insights into the ecological factors underlying the origins and maintenance of diversity. Larvae of sunflower maggot flies in genus Strauzia feed on the pith of plants in the family Asteraceae. Although Strauzia tend to be host specialists, some species overlap in their host use. To resolve the origins of host sharing among these specialist flies, we used reduced representation genomic sequencing to infer the first multi-locus phylogeny of genus Strauzia. Our results show that Helianthus tuberosus and Helianthus grosseserratus each host three different fly species, and that the flies co-occurring on a host are not one another’s closest relatives. Though this pattern implies that host sharing is most likely the result of host shifts, these may not be host shifts in the conventional sense of an insect moving onto an entirely new plant. Many hosts of Strauzia belong to a young (1-2 MYA) clade of perennial sunflowers noted for their frequent introgression and hybrid speciation events. In at least one case, flies may have converged upon a host after their respective ancestral host plants hybridized to form a new sunflower species (H. tuberosus). Broadly, we suggest that rapid and recent adaptive introgression and speciation in this group of plants may have instigated the diversification of their phytophagous fly associates, including the convergence of >1 species onto the same shared host plants.

The D genome progenitor of bread wheat, Aegilops tauschii Cosson (DD, 2n = 2x = 14), which is naturally distributed in Central Eurasia, ranging from northern Syria and Turkey to western China, is considered a potential genetic resource for improving bread wheat. In this study, the chloroplast (cp) genomes of 17 Ae. tauschii accessions were reconstructed. The cp genome sizes ranged from 135,551 bp to 136,009 bp and contained a typical quadripartite structure of angiosperms. Within these genomes, we identified a total of 124 functional genes, including 82 protein-coding genes, 34 transfer RNA genes and eight ribosomal RNA genes, with 17 duplicated genes in the IRs. Although the comparative analysis revealed that the genomic structure (gene order, gene number and IR/SC boundary regions) is conserved, a few variant loci were detected, predominantly in the non-coding regions (intergenic spacer regions). The phylogenetic relationships determined based on the complete genome sequences were consistent with the hypothesis that Ae. tauschii populations in the Yellow River region of China originated in South Asia not Xinjiang province or Iran, which could contribute to more effective utilization of wild germplasm resources. Furthermore, we confirmed that Ae. tauschii was derived from monophyletic speciation rather than hybrid speciation at the cp genome level. We also identified four variable genomic regions, rpl32-trnL-UAG, ccsA-ndhD, rbcL-psaI and rps18-rpl20, showing high levels of nucleotide polymorphisms, which may accordingly prove useful as cpDNA markers in studying the intraspecific genetic structure and diversity of Ae. tauschii.

Background and AimsHybridization is commonly assumed to aid invasions through adaptive introgression. In contrast, a recent theoretical model predicted that there can be non-adaptive demographic advantages from hybridization and that the population consequences will depend on the breeding systems of the species and the extent to which subsequent generations are able to interbreed and reproduce. We examined cross-fertilization success and inheritance of breeding systems of two species in order to better assess the plausibility of the theoretical predictions.MethodsReciprocal artificial crosses were made to produce F1, F2 and backcrosses between Cakile maritima (self-incompatible, SI) and Cakile edentula (self-compatible, SC) (Brassicaceae). Flowers were emasculated prior to anther dehiscence and pollen was introduced from donor plants to the recipient’s stigma. Breeding system, pollen viability, pollen germination, pollen tube growth and reproductive output were then determined. The results were used to replace the assumptions made in the original population model and new simulations were made.Key ResultsThe success rate with the SI species as the pollen recipient was lower than when it was the pollen donor, in quantitative agreement with the ‘SI × SC rule’ of unilateral incompatibility. Similar outcomes were found in subsequent generations where fertile hybrids were produced but lower success rates were observed in crosses of SI pollen donors with SC pollen recipients. Much lower proportions of SC hybrids were produced than expected from a single Mendelian allele. When incorporated into a population model, these results predicted an even faster rate of replacement of the SC species by the SI species than previously reported.ConclusionsOur study of these two species provides even clearer support for the feasibility of the non-adaptive hybridization hypothesis, whereby the colonization of an SI species can be assisted by transient hybridization with a congener. It also provides novel insight into reproductive biology beyond the F1 generation.

Hybrid speciation is an important way to generate species diversity. In general, however, interspecific hybridization is easily confused with the formation of hybrid species. Using the genomic resequencing data of the kiwifruit genus (Actinidia), at least ten species were documented recently as homoploid hybrid species, and thus a two-layer mode of species diversification has been proposed. As a crucial piece of evidence, Actinidia fulvicoma was identified as a hybrid derivative of Actinidia eriantha × Actinidia cylindrica, representing a rare case of hybrid species in kiwifruit that won the competition of ecological niches with one of its putative parental species, A. cylindrica. However, the hypothesized hybrid origin of A. fulvicoma is inconsistent with our specimen observations. Here, we present multiple lines of evidence to reject the hybrid speciation hypothesis for this species, despite genomic evidence for frequent interspecific gene flow. We collected the samples of A. fulvicoma in type locality and neighboring regions to contrast them with type specimen, and sequenced nuclear ribosomal DNA ITS, chloroplast trnL-trnF and mitochondrial nad2-i3, as well as four single-copy nuclear genes explored from kiwifruit genomes, to infer phylogenetic relationships among A. fulvicoma, its putative parental species, and their relatives. Our data definitely reveal that A. fulvicoma occupies an independent backbone lineage and it is not a hybrid. This study suggests that correct evolutionary applications on extensive surveys of the putative hybrid and its possible parents with strict criteria are necessary in the documentation of hybrid speciation to advance our understanding of the genomic basis of hybrid species.

It has long been recognized that hybridization and polyploidy are prominent processes in plant evolution. Although classically recognized as significant in speciation and adaptation, recognition of the importance of interspecific gene flow has dramatically increased during the genomics era, concomitant with an unending flood of empirical examples, with or without genome doubling. Interspecific gene flow is thus increasingly thought to lead to evolutionary innovation and diversification, via adaptive introgression, homoploid hybrid speciation and allopolyploid speciation. Less well understood, however, are the suite of genetic and genomic mechanisms set in motion by the merger of differentiated genomes, and the temporal scale over which recombinational complexity mediated by gene flow might be expressed and exposed to natural selection. We focus on these issues here, considering the types of molecular genetic and genomic processes that might be set in motion by the saltational event of genome merger between two diverged species, either with or without genome doubling, and how these various processes can contribute to novel phenotypes. Genetic mechanisms include the infusion of new alleles and the genesis of novel structural variation including translocations and inversions, homoeologous exchanges, transposable element mobilization and novel insertional effects, presence-absence variation and copy number variation. Polyploidy generates massive transcriptomic and regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory factors, small RNAs and other genome interactions that cascade from single-gene expression change up through entire networks of transformed regulatory modules. We highlight both these novel combinatorial possibilities and the range of temporal scales over which such complexity might be generated, and thus exposed to natural selection and drift., This study was supported by the grants CGL2017-88500-P (AEI/FEDER, EU) to GN and AGL2016-78992-R to JC from the Spanish Ministry of Economy and Competitivity, as well as Severo Ochoa Program for Centers of Excellence in R&D 2016–2020 (SEV-2015-0533) to JC, and by grants from the National Science Foundation to JW.

The diploid D-genome lineage of the Triticum/Aegilops complex has an evolutionary history involving genomic contributions from ancient A- and B/S-genome species. We explored here the possible cytonuclear evolutionary responses to this history of hybridization. Phylogenetic analysis of chloroplast DNAs indicates that the D-genome lineage has a maternal origin of the A-genome or some other closely allied lineage. Analyses of the nuclear genome in the D-genome species Aegilops tauschii indicate that accompanying and/or following this ancient hybridization, there has been biased maintenance of maternal A-genome ancestry in nuclear genes encoding cytonuclear enzyme complexes (CECs). Our study provides insights into mechanisms of cytonuclear coevolution accompanying the evolution and eventual stabilization of homoploid hybrid species. We suggest that this coevolutionary process includes likely rapid fixation of A-genome CEC orthologs as well as biased retention of A-genome nucleotides in CEC homologs following population level recombination during the initial generations.

Picea purpurea originated from the homoploid hybrid speciation, which occupy novel alpine habitats in the north-east region of the Qinghai-Tibet Plateau (QTP) where its progenitors, P. wilsonii and P. likiangensis are excluded. Alpine habitats are usually characterized by low atmospheric CO2 concentrations and strong solar radiation with a large fraction of shortwave radiation (i.e. blue light). To test whether P. purpurea has the transgressive segregation in photosynthetic capacity and stomatal characteristics contributed to occupying such extreme habitats, we investigated the leaf gas exchange properties at two level of CO2 concentration (Ca: 200 and 400 μmol mol−1), light responsive curves of photosynthesis under three light qualities (red, blue and a mixture of both red and blue light at the ratio of 94:6), stomatal and other relative physiological traits for all three species. Our results show evidence of transgressive segregation in hybrid species; for instance, under blue and red light P. p...

Significance Hybridization can promote speciation, and examples of putative hybrid species have now been identified across the tree of life. However, we still know little about the conditions that are most conducive to hybrid speciation. We have used experimental evolution in fruit flies (Drosophila) to show that both the genetic difference between hybridizing species and the number of hybridizing species affect the probability that hybrids evolve reproductive isolation from their parental species. Our results provide a systematic test of factors that affect homoploid hybrid speciation. Biologists will now be able to test the predictions that our experiments outline in naturally hybridizing species. These types of data hold the potential to greatly increase our understanding of hybridization’s role in generating biodiversity., Hybridization is often maladaptive and in some instances has led to the loss of biodiversity. However, hybridization can also promote speciation, such as during homoploid hybrid speciation, thereby generating biodiversity. Despite examples of homoploid hybrid species, the importance of hybridization as a speciation mechanism is still widely debated, and we lack a general understanding of the conditions most likely to generate homoploid hybrid species. Here we show that the level of genetic divergence between hybridizing species has a large effect on the probability that their hybrids evolve reproductive isolation. We find that populations of hybrids formed by parental species with intermediate levels of divergence were more likely to mate assortatively, and discriminate against their parental species, than those generated from weakly or strongly diverged parental species. Reproductive isolation was also found between hybrid populations, suggesting differential sorting of parental traits across populations. Finally, hybrid populations derived from three species were more likely to evolve reproductive isolation than those derived from two species, supporting arguments that hybridization-supplied genetic diversity can lead to the evolution of novel “adaptive systems” and promote speciation. Our results illustrate when we expect hybridization and admixture to promote hybrid speciation. Whether homoploid hybrid speciation is a common speciation mechanism in general remains an outstanding empirical question.

Genomic data are a powerful tool for elucidating the processes involved in the evolution and divergence of species. The speciation and phylogenetic relationships among Chinese Juglans remain unclear. Here, we used results from phylogenomic and population genetic analyses, transcriptomics, Genotyping-By-Sequencing (GBS), and whole chloroplast genomes (Cp genome) data to infer processes of lineage formation among the five native Chinese species of the walnut genus (Juglans, Juglandaceae), a widespread, economically important group. We found that the processes of isolation generated diversity during glaciations, but that the recent range expansion of J. regia, probably from multiple refugia, led to hybrid formation both within and between sections of the genus. In southern China, human dispersal of J. regia brought it into contact with J. sigillata, which we determined to be an ecotype of J. regia that is now maintained as a landrace. In northern China, walnut hybridized with a distinct lineage of J. mandshurica to form J. hopeiensis, a controversial taxon (considered threatened) that our data indicate is a horticultural variety. Comparisons among whole chloroplast genomes and nuclear transcriptome analyses provided conflicting evidence for the timing of the divergence of Chinese Juglans taxa. J. cathayensis and J. mandshurica are poorly differentiated based our genomic data. Reconstruction of Juglans evolutionary history indicate that episodes of climatic variation over the past 4.5 to 33.80 million years, associated with glacial advances and retreats and population isolation, have shaped Chinese walnut demography and evolution, even in the presence of gene flow and introgression.

Ocbil theory was developed to better understand the origins, ecology and conservation of biodiversity and cultural diversity on the Earth's oldest, climatically buffered, most infertile landscapes (Ocbils), which are especially prominent in the Southwest Australian and Greater Cape Floristic Regions. Natural hybridization involves the mating of individuals from distinguishable populations, usually of distinct taxa, and often involves the production of later-generation derivatives from such matings. Drawing upon Edgar Anderson's Hybridized Habitat hypothesis and Arnold's modern development of Anderson's and Stebbins' ‘genetic exchange in fluctuating environments’ thesis, it is predicted that natural hybridization, introgression and hybrid speciation will be reduced in Ocbils and more common in Yodfels (young, often-disturbed, fertile landscapes) globally – the Reduced Hybridization Hypothesis for Ocbils. Evidence supporting this hypothesis is explored in herbarium and field data on hybridization rates and hybrid speciation in southwest Australia, contrasted with reviews of hybridization rates in other global regions. Further research is recommended and independent tests in South Africa and other countries with Ocbils would be instructive. The solitary Ocbil dwelling Eucalyptus × graniticola Hopper is described in supplementary material to exemplify the Reduced Hybridization Hypothesis.

Using the study of hybridization in evolutionary biology as metaphorical inspiration, I offer a thought experiment about the emergence and proliferation of social enterprise and the influence of hybrid organizing on the entrepreneurial ecosystem. After establishing a number of analogues between biological and organizational hybrids, I analyze the degree to which social enterprise may be indicative of hybrid speciation – i.e., a new organizational form – versus introgressive hybridization – i.e., a variant of a more traditional organizational form. I then use the metaphor to examine whether social enterprise: (1) possesses distinct rules and features, (2) is shaped by or shaping the entrepreneurial ecosystem, (3) still remains a hybrid organization, and (4) might even be considered an invasive species.

The analysis of hybridization and gene flow among closely related taxa is a common goal for researchers studying speciation and phylogeography. Many methods for hybridization detection use simple site pattern frequencies from observed genomic data and compare them to null models that predict an absence of gene flow. The theory underlying the detection of hybridization using these site pattern probabilities exploits the relationship between the coalescent process for gene trees within population trees and the process of mutation along the branches of the gene trees. For certain models, site patterns are predicted to occur in equal frequency (i.e., their difference is 0), producing a set of functions called phylogenetic invariants. In this paper we introduce HyDe, a software package for detecting hybridization using phylogenetic invariants arising under the coalescent model with hybridization. HyDe is written in Python, and can be used interactively or through the command line using pre-packaged scripts. We demonstrate the use of HyDe on simulated data, as well as on two empirical data sets from the literature. We focus in particular on identifying individual hybrids within population samples and on distinguishing between hybrid speciation and gene flow. HyDe is freely available as an open source Python package under the GNU GPL v3 on both GitHub (https://github.com/pblischak/HyDe) and the Python Package Index (PyPI: https://pypi.python.org/pypi/phyde).

Despite examples of homoploid hybrid species, theoretical work describing when, where, and how we expect homoploid hybrid speciation to occur remains relatively rare. Here I explore the probability of homoploid hybrid speciation due to “symmetrical incompatibilities” under different selective and genetic scenarios. Through simulation, I test how genetic architecture and selection acting on traits that do not themselves generate incompatibilities interact to affect the probability that hybrids evolve symmetrical incompatibilities with their parent species. Unsurprisingly, selection against admixture at ‘adaptive’ loci that are linked to loci that generate incompatibilities tends to reduce the probability of evolving symmetrical incompatibilities. By contrast, selection that favors admixed genotypes at adaptive loci can promote the evolution of symmetrical incompatibilities. The magnitude of these outcomes is affected by the strength of selection, aspects of genetic architecture such as linkage relationships and the linear arrangement of loci along a chromosome, and the amount of hybridization following the formation of a hybrid zone. These results highlight how understanding the nature of selection, aspects of the genetics of traits affecting fitness, and the strength of reproductive isolation between hybridizing taxa can all be used to inform when we expect to observe homoploid hybrid speciation due to symmetrical incompatibilities.

Rapid hybrid speciation in Darwin's finches Galapagos finches have driven hypotheses of how speciation occurs. Most commonly, it is assumed that natural selection separates species originating from a single population on the basis of variation in traits that confer advantages for survival and reproduction. Lamichhaney et al. document a case where cross-species hybridization established a reproductively isolated lineage, which demonstrates a process known as homoploid hybrid speciation in action (see the Perspective by Wagner). The authors used genetic markers and phenotypic analyses to create a pedigree that revealed how a cross-island migrant bred with a native species to form a self-perpetuating hybrid population that was reproductively isolated from both parental species. Science , this issue p. 224 ; see also p. 157