# PLOS/Eukaryote hybrid genomes

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Published in PLOS Genetics Adapted for English Wikipedia Public peer review comments can be seen here Published under Creative Commons License CC BY 4.0 10.1371/journal.pgen.1008404

## Abstract

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adapation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve.

## Background

Genetic exchange between species can impede the evolution of biodiversity because gene flow between diverging species counteracts their differentiation and hybridization between recently diverged species can lead to loss of genetic adaptations or species fusion. Traditionally, zoologists have viewed interspecific hybridization as maladaptive behaviour which can result in breaking up co-adapted gene complexes. In contrast, plant biologists recognized early on that hybridization can sometimes be an important evolutionary force, contributing to increasing biodiversity. Recently, evidence has been accumulating showing that hybridization is also an important evolutionary process in animals. Interspecific hybridization can enrich the genetic diversity of introgressed taxon, lead to introgression of beneficial genetic variation or even generate new hybrid species. Hybridization is now also known to contribute to the evolutionary potential in several textbook examples of adaptive radiation, including the Geospiza Galapagos finches, African cichlid fishes, Heliconius butterflies and Hawaiian Madiinae tarweeds and silverswords. Here we review the evolutionary outcomes of interspecific hybridization and the properties of genomes of hybrid genomes. Many of the discussed topics also apply to hybridization between different subspecies or populations of the same species, but here we focus on interspecific hybridization (referred to as hybridization in this review).

## Evolutionary outcomes of hybridization

There are several potential evolutionary outcomes of hybridization (Fig. 1). If early generation hybrids are not viable or sterile, hybridization may reduce the reproductive success of the parent species. This could potentially lead to reinforcement, selection to strengthen premating isolation or if the species fail to evolve premating isolation, it could increase their extinction risk due to wasted reproductive effort. If the fitness of early generation hybrids is non-zero and that of some later generation hybrids is as high or even higher than the fitness of one or both parent taxa, hybrids may displace the parent taxa and the hybridizing taxa may fuse (speciation reversal; Fig. 1). If the fitness of early generation hybrids is reduced but non-zero, hybrid zones may emerge in the contact zone of the taxa. If hybrids are fertile, hybridization may contribute novel variation through rare hybrids backcrosssing with parental species. Such introgressive hybridization may enable neutral or selectively beneficial alleles to be transferred across species boundaries even in species pairs that remain distinct despite occasional gene flow. Hybrid fitness may vary with divergence time between the hybridizing taxa. This pattern has been shown for a variety of taxa including Drosophila, birds and fish. Hybrid fitness may also differ with cross direction, between first generation and later generation hybrids, and among individuals within generations of the same cross-type. In some cases hybrids may evolve into new hybrid species with reproductive isolation to both parent taxa. Below we describe the evolutionary outcomes of hybridisation that result in persistent hybrid genomes.

## Adaptive introgression

When rare hybrids backcross with parent species alleles coding for traits that are beneficial for both parental species can be transferred across species boundaries, even if parent species remain distinct taxa. This process is referred to as adaptive introgression (a somewhat misleading term because backcrossing itself may not be adaptive, but some of the introgressed variants may be beneficial.) Simulations suggest that adaptive introgression is possible unless hybrid fitness is substantially reduced, or the adaptive loci are tightly linked to deleterious ones. Examples of adaptive traits that have been transferred via introgression include an insecticide resistance gene that was transferred from Anopheles gambiae to A. coluzzii and the red warning wing colouration trait in Heliconius butterflies that is under natural selection from predators which has been introgressed from e.g. H. melpomene to H. timareta and other Heliconius species. In the plant Arabidopsis arenosa some of the alleles conferring adaptation to drought and phytotoxic levels of metal have been introgressed from A. lyrata. Even in humans there is evidence for adaptive introgression of e.g. immunity alleles, skin pigmentation alleles and alleles conferring adaptation to high altitude environments from Neanderthal and Denisovans. If traits important for species recognition or reproductive isolation introgress into a population of another species, the introgressed population may become reproductively isolated against other populations of the same species. Examples of this include Heliconius butterflies, where selective introgression of wing pattern genes between diverged lineages occurs (see e.g.), and wing patterns contribute to reproductive isolation in some species pairs with low (e.g. between H. t. florencia and H. t. linaresi) and intermediate levels (e.g. H. c. galanthus/H. pachinus) of divergence.

## What is a hybrid species?

One of the potential evolutionary outcomes of hybridisation is the establishment of a novel, reproductively isolated lineage, i.e., hybrid speciation. A hybrid species has an admixed genome and forms stable genetically distinct populations. Some researchers argue that evidence of a hybridization-derived basis for reproductive isolation should be an additional defining criterion for hybrid speciation, but see. This stricter definition includes polyploid hybrid taxa but only encompasses a handful of well studied cases of homoploid hybrid speciation, e.g. Heliconius heurippa, Passer italiae, and three Helianthus sunflower species because for most suggested examples of homoploid hybrid speciation, the genetic basis of reproductive isolation is still unknown.
Hybrid species can occupy an ecological niche different to those of the parents and may be isolated from the parent species primarily through pre-mating barriers (hybrid speciation with external barriers, c.f.). Hybrid species may also be reproductively isolated from the parent species through sorting of incompatibilities leading to new combinations of parental alleles that are incompatible with both parent species but compatible within the hybrid taxon (recombinational hybrid speciation). A recombinational hybrid taxon typically also has a substantial proportion of the genome derived from the donor of introgressed material, although variation exists both between taxa and within lineages of hybrid taxa (see e.g.).

## Homoploid and polyploid hybrid speciation

In general, hybrid species can arise from two major types of hybrid speciation, defined by whether the speciation event is associated with genome duplication (polyploidy) or not. Homoploid hybrid speciation Homoploid hybrid speciation is defined as the evolution of a new hybrid species with reproductive isolation to both parent taxa without change of ploidy, i.e. number of chromosome sets (Fig. 2). The genomes of homoploid hybrid species are mosaics of the parent genomes as ancestry tracts from the parent species are broken up by recombination. In the case of polyploid hybrid speciation, hybridisation is associated with genome duplication, resulting in an allopolyploid with increased ploidy compared to their parental taxa (Fig. 2). In contrast to allopolyploids, autopolyploids are characterised by genome duplication within the same species and are thus not discussed further in the context of this review. Allopolyploid speciation is more common in plants than in animals. Polyploid hybrids can be instantly isolated from their parental species through chromosome number differences.

## Reproductive isolation against parent species

Sufficient reproductive isolation from both parental species is required for the successful establishment of a hybrid species. Reproductive isolation against parent species is harder to achieve for homoploid hybrids where karyotype differences do not contribute to intrinsic isolation. Reproductive isolation between a hybrid species and its parental species can arise from a variety of reproductive barriers either before or after fertilization (prezygotic or postzygotic, respectively), which may themselves be dependent or independent of environmental conditions (extrinsic or intrinsic barriers, respectively). For example, intrinsic postzygotic barriers cause hybrid inviability or sterility regardless of the environment in which they occur, while extrinsic postzygotic barriers result in hybrids of low fitness due to maladaptation to specific environments.
Prezygotic intrinsic and extrinsic differences have also been shown to be important in isolating hybrids from their parent species. In plants, pollinator mediated isolation resulting from changes in floral characteristics may be an important extrinsic prezygotic ecological barrier. Strong extrinsic pre-zygotic has been shown to isolate the hybrid species Senecio eboracensis from its parent species, where hybrids are virtually absent in the wild, although a fraction of hybrid offspring are fertile in lab experiments. Lowe & Abbott conclude that selfing, timing of flowering and characters involved in pollinator attraction likely contribute to this external isolation. Prezygotic mate preference driven isolation generated from intrinsic assortative mating between hybrids has also been reported in several taxa. In African cichlid fish, experimental hybrids displayed combinations of parental traits and preferences which resulted in hybrids predominantly mating with other hybrids. A similar pattern was found in Geospiza Galapagos finches where a specific hybrid song resulted from the transgressive beak morphology, and hybrid Heliconius butterflies preferred the hybrid wing patterning over that of both parent species. Intrinsic differences in habitat use or in phenology may result in some degree of reproductive isolation against parent species if mating is time and habitat-specific. For example the apple host race in Rhagoletis pomonella maggot flies evolved after introgression of diapause related genes from Mexican altiplano flies that allowed a switch from the ancestral host hawthorne to the later flowering apple and isolated the two host races via allochronic intrinsic pre-zygotic isolation. In Xiphophorus swordtail fish strong ancestry assortative mating maintained a hybrid genetic cluster separate for 25 generations, but disappeared under manipulated conditions. Hence, prezygotic reproductive barriers to gene flow may be environment dependent.
Postzygotic isolating barriers have also been shown to be important in a variety of hybrid lineages. Work on Helianthus sunflowers has revealed that intrinsic postzygotic can cause reproductive isolation against the parent species. The postzygotic barriers consist in pre-existing structural differences, in combination with hybridization induced structural differences. Sorting of incompatibilities between parent species, where one subset of these isolates the hybrid taxon against one parent and a different subset isolates it against the other parent, has resulted in intrinsic postzygotic isolation between the Italian sparrow Passer italiae and its parent species. Simulation studies show that the likelihood of hybrid speciation through this mechanism depends on the divergence time between parent species, the population size of the hybrid species, the nature of selection acting on hybrids, and linkage among incompatibilities to each other and to adaptive variants. Extrinsic ecological barriers against parent species may arise as by-products of ecological differentiation if mating is time and/or habitat specific. Hybrid species have been shown to adapt to novel ecological niches through transgressive phenotypes, or through novel combinations of ecological traits from the parent species, and ecological selection against parent-hybrid cross phenotypes would result in extrinsic postzygotic isolation.

## Stabilization of hybrid genomes

Hybridization can have many different outcomes. Hybrid speciation results in reproductive isolation against both parent species and genomes that evolve independently from those of the parent species. Introgressive hybridization can transfer important novel variants into genomes of a species that remains distinct from the other taxa in spite of occasional gene flow. Here we refer to both types of hybridization-derived genomes as persistent hybrid genomes. Following initial hybridization, introgression tracts, the genetic blocks inherited from each parent species, are broken down with successive generations and recombination events. Recombination is more frequent in homoploid hybrid genomes than in allopolyploid hybrid genomes. In allopolyploids, recombination can destabilize the karyotype and lead to aberrant meiotic behaviour and reduced fertility, but may also generate novel gene combinations and advantageous phenotypic traits as in homoploid hybrids. Once hybridization between the hybrid taxon and its parent taxa ceases, different ancestry blocks or introgression tracts may become fixed, a process referred to as "genome stabilization". Some introgression tracts are removed by selection against incompatibilities and others are fixed. Theoretical models on hybrid zones suggest that the breakdown of ancestry blocks through recombination is suppressed near genes conferring reproductive isolation due to lower fitness of recombinant hybrids. The strength of the suppression is affected by the form of selection, dominance, and whether the locus was situated on an autosome or sex chromosome. The time to genome stabilization is variable. Fixation of ancestry blocks was found to be rapid in experimental hybrid Helianthus sunflower species genomes, and the genome stabilization of hybrid sunflower species is estimated to take hundreds of generations. In Zymoseptoria fungi genomes were stabilized within ca. 400 generations, whereas in hybrid Xiphophorus swordtail genomes genome stabilization was not achieved until after ca. 2000 and 2500 generations. Few Neanderthal regions have fixed in human genomes during the ca. 2000 generations after hybridization, and segregating incompatibilities are present in the hybrid Italian sparrow approximately 5000 generations after the initial hybridization event.
Given time, genetic drift will eventually stochastically fix blocks derived from the two parent species in finite isolated hybrid populations. Selection against incompatibility loci may accelerate the process of fixation of parental alleles as hybrids that possess alleles that are less likely to cause incompatibility will have higher fitness and favourable alleles will spread in the population. Fixation of recessive weakly deleterious alleles in the parent taxa may, however, also result in hybrids retaining both parental alleles: because hybrids with haplotypes from both parents are not homozygous for any weakly deleterious alleles, they have higher fitness than hybrids with only one parental haplotype. This associative overdominance, may slow down the process of fixation of parental alleles through favouring retention of both parental haplotypes. The effect of associative overdominance is strongest in low recombination regions, including inversions. The balance between alleles and allelic combinations providing favourable phenotypic characters and the strength of selection against incompatibilities determine what introgression tracts will be inherited from which parent species upon hybridization (Fig.3). An insecticide resistance region was retained following a hybridization event in Anopheles coluzzi, suggesting a role for selection in maintaining favourable introgressed regions. The local recombination rate is important for the likelihood of introgression because in the case of widespread incompatibilities, introgressed alleles are more likely to recombine away from incompatibilities in high recombination regions. This pattern has been detected in monkeyflowers Mimulus, in Mus domesticus house mice, in Heliconius butterflies and in Xiphophorus swordtail fish.
Genome-wide incompatibilities have been identified in Xipophorous fish, chimeric genes and mutations of orthologous genes cause incompatibilities in early generation experimental Cyprinidae goldfish - carp hybrids and mito-nuclear incompatibilies are found to have a key role e.g. in Italian sparrows, fungus and cyto-nuclear incompatibilities in Mimulus plants. Evidence from altered expression patterns in synthetic hybrids and missing gene combinations in a hybrid species also suggest that DNA-repair and genes involved in mutagenesis and cancer related pathways may cause incompatibilities in hybrids. Genome formation in hybrid species is shaped by selection against incompatible combinations.

## Altered genome properties in hybrid taxa

The hybrid origin may affect genome structure and properties. It has been shown to increase mutation rates, to activate transposable elements, and to induce chromosomal rearrangements. Increased transposon activation, as proposed in McClintock's ‘genomic shock’ theory, could result in alterations to gene expression. Transposable elements may, in addition to altering gene products if inserted into a gene, also alter promoter activity for genes if inserted upstream of the coding regions, or may induce gene silencing as a result of gene disruption. For allopolyploid genomes chromosomal rearrangements may result from the ”genomic shock” induced by hybridisation, with more distantly related species being more prone to genome reorganisations e.g. in Nicotiana. Chromosomal rearrangements resulting from either genomic shock or recombination events between non-homologous subgenomes may cause genome sizes to either increase or decrease. Both increases and decreases were found in the Nicotiana genus, and were not related to the age since hybridization.
Following genome duplication in allopolyploids, the genome goes through diploidization, which is a process in which the genome is rearranged to act as a meiotic diploid. After such diploidization, much of the genome is lost due to genome fractionation, the loss-of-function of one or the other of the newly duplicated genes. In a meta analysis, Sankoff and collaborators found evidence consistent with reduction-resistant pairs and a concentration of functional genes on a single chromosome and suggest that the reduction process partly is constrained.
A related allopolyploid specific phenomenon is subgenome dominance. For example, in the octoploid Fragaria strawberry, one of the four subgenomes is dominant and has significantly greater gene content, more frequently has its genes expressed, and exchanges between homologous chromosomes are biased in favour of this subgenome, as compared with the other subgenomes. This study also showed that certain traits, e.g. disease-resistance, are controlled by the dominant subgenome to a high extent. A proposed mechanism of how subgenome dominance arises, suggests that relative dominance is related to the density of transposable elements in each subgenome. Subgenomes with higher transposable element density tend to behave submissively relative to the other subgenomes when brought together in the allopolyploid genome. Interestingly, subgenome dominance can arise immediately in allopolyploids, as shown in synthetic and recently evolved monkeyflowers.
In addition to these changes to genome structure and properties, studies of allopolyploid rice and whitefish suggest that patterns of gene expression may be disrupted in hybrid species. Studies of synthetic and natural allopolyploids of Tragopogon miscellus show that gene expression is less strictly regulated directly after hybridization, and that novel patterns of expression emerge and are stabilized during 40 generations. While expression variation in miRNAs alters gene expression and affects growth in the natural allopolyploid Arabidopsis suecica and experimental lineages, inheritance of siRNAs is stable and maintains chromatin and genome stability, potentially buffering against a transcriptomic shock.

## What factors influence the likelihood of the formation of persistent hybrid genomes?

Whereas hybridization is required for the generation of persistent hybrid genomes, it is not sufficient. For the persistence of hybrid genomes in hybrid species they need to be sufficiently reproductively isolated from their parent species to avoid species fusion. Selection on introgressed variants allows the persistence of hybrid genomes in introgressed lineages. Frequency of hybridization, viability of hybrids, and the ease at which reproductive isolation against the parent species arises or strength of selection to maintain introgressed regions are hence factors influencing the rate of formation of stable hybrid lineages.
Few general conclusions about the relative prevalence of hybridization can be drawn, as sampling is not evenly distributed, even if there is evidence for hybridization in an increasing number of taxa. One pattern that emerges is that hybridization is more frequent in plants where it occurs in 25% of the species, whereas it only occurs in 10% of animal species. Most plants, as well as many groups of animals, lack heteromorphic sex chromosomes. The absence of heteromorphic sex chromosomes results in slower accumulation of reproductive isolation, and may hence enable hybridization between phylogenetically more distant taxa. Haldane's rule states that ”when F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous sex”. Empirical evidence supports a role for heteromorphic sex chromosomes in hybrid sterility and inviability. A closely related observation is the large X effect stating that there is a disproportionate contribution of the X/Z-chromosome in fitness reduction of heterogametic hybrids. These patterns likely arise as recessive alleles with deleterious effects in hybrids have a stronger impacts on the heterogametic than the homogametic sex, due to hemizygous expression. In taxa with well-differentiated sex chromosomes, Haldane’s rule has shown to be close to universal, and heteromorphic sex chromosomes show reduced introgression on the X in XY (see for a review). In line with a role for heteromorphic sex chromosomes in constraining hybrid genome formation, elevated differentiation on sex chromosomes has been observed in both ZW and XY systems. This pattern may reflect the lower effective population sizes and higher susceptibility to drift on the sex chromosomes, the elevated frequency of loci involved in reproductive isolation and/or the heightened conflict on sex chromosomes. Findings of selection for uniparental inheritance of e.g. mitonuclear loci residing on the Z chromosome in hybrid Italian sparrows is consistent with compatible sex chromosomes being important for the formation of a viable hybrid genomes.
There are also several ecological factors that affect the probability of hybridization. Generally, hybridization is more frequently observed in species with external fertilization including plants but also fishes, than in internally fertilized clades. In plants, high rates of selfing in some species may prevent hybridization, and breeding system may also affect the frequency of heterospecific pollen transfer. In fungi, hybrids can be generated by ameiotic fusion of cells or hyphae in addition to mechanisms available to plants and animals. Such fusion of vegetative cells and subsequent parasexual mating with mitotic crossover may generate recombined hybrid cells.
For hybrid species to evolve, reproductive isolation against the parent species is required. The ease by which such reproductive isolation arises is thus also important for the rate at which stable hybrid species arise. Polyploidisation and asexuality are both mechanisms that result in instantaneous isolation and may increase the rate of hybrid lineage formation. The ability to self-pollinate may also act in favour of stabilising allopolyploid taxa by providing a compatible mate (itself) in the early stages of allopolyploid speciation when rare cytotypes are at a reproductive disadvantage due to inter-cytotype mating. Selfing is also expected to increase the likelihood of establishment for homoploid hybrids according to a modelling study, and the higher probability of selfing may contribute to the higher frequency of hybrid species in plants. Fungal hybridization may result in asexual hybrid species, as Epichloe fungi where hybrids species are asexual while nonhybrids include both asexual and sexual species. Hybridization between strongly divergent animal taxa may also generate asexual hybrid species, as shown e.g. in the European spined loaches, Cobitis, and most if not all asexual vertebrate species are of hybrid origin. Interestingly, Arctic floras harbour an unusually high proportion of allopolyploid plants, suggesting that these hybrid taxa could have an advantage in extreme environments, potentially through reducing the negative effects of inbreeding. Hence both genomic architecture and ecological properties may affect the probability of hybrid species formation.
For introgressed taxa, the strength of selection on introgressed variants decides whether introgressed sections will spread in the population and stable introgressed genomes will be formed. Strong selection for insecticide resistance has been shown to increase introgression of an Anopheles gambiae resistance allele into A. coluzzi malaria mosquitoes. In Heliconius butterflies, strong selection on having the locally abundant wing colour patterns repeatedly led to fixation of alleles that introgressed from locally adapted butterflies into newly colonizing species or subspecies. Chances of fixation of beneficial introgressed variants depend on the type and strength of selection on the introgressed variant and linkage with other introgressed variants that are selected against.

## What genes and genomic regions are affected by hybridization?

Genetic exchange can occur between populations or incipient species diverging in geographical proximity or between divergent taxa that come into secondary contact. Hybridization between more diverged lineages is expected to have a greater potential to contribute beneficial alleles or generate novelty than hybridization between less diverged populations because more divergent alleles are combined, and are thus more likely to have a large fitness effect, to generate transgressive phenotypes. Hybridization between more diverged lineages is also more likely to generate incompatible allele combinations, reducing initial hybrid fitness but potentially also contributing to hybrid speciation if they are sorted reciprocally as described above. An intermediate genetic distance may thus be most condusive to hybrid speciation. Experimental lab crosses support this hypothesis.
The proportion of the genome that is inherited from the recipient of introgressed material varies strongly among and within species. After the initial hybridization event the representation is 50% in many polyploid taxa, although parental gene copies are successively lost and might bias the contribution to one majority parent genome. Relatively equal parental contributions are also found in some homoploid hybrid species but in other cases they are highly unequal such as in some Heliconius species. The majority ancestry may even be that from the donor of introgressed material, as was shown for Anopheles gambiae mosquitoes. Interestingly there may also be variation in parental contribution within a hybrid species. In both swordtail fish and Italian sparrows there are populations which differ strongly in what proportions of the parent genomes they have inherited.
Patterns of introgression can vary strongly across the genome, even over short chromosomal distances. Examples of adaptive introgression of well defined regions, include an inversed region containing genes involved in insecticide resistance and introgression of a divergent, inverted chromosomal segment has resulted in a ”super gene” that encodes mimicry polymorphism in the butterfly Heliconius numata. These findings are consistent with models suggesting that genomic rearrangements are important for the coupling of locally adaptive loci. Genes and genomic regions that are adaptive may be readily introgressed between species e.g. in hybrid zones if they are not linked to incompatibility loci. This often referred to semi-permeable species boundaries, and examples include e.g. genes involved in olfaction that are introgressed across a Mus musculus and M. domesticus hybrid zone. In hybrid zones with mainly permeable species boundaries, patterns of introgressed regions enable deducing what genomic regions involved in incompatibilities and reproductive isolation c.f.

## Conclusions and future directions

Hybridization is a common phenomenon with a wide range of consequences. These include both the formation of novel hybrid species, which are reproductively isolated from their parent species and where the admixed genomes undergo independent evolution, and introgression of adaptive variants across species boundaries in species that remain distinct in spite of occasional gene flow. The divergent genetic material in admixed genomes of hybrid taxa enables adaptation to novel environments and niches. When the divergent genomes of two species come together, incompatible combinations may reduce fitness. As hybrid genomes are frequently observed, the advantage of novel adaptive trait combinations can sometimes override potential negative effects from incompatibilities and enable hybrid lineages to purge these incompatibilities during the process of genome stabilization.
While the last decades have provided ample evidence for that hybrid genome formation is common and contributes novel species and enables adaptation, many questions remain. How long does it take for a hybrid genome to stabilize and why is there variation in time to genome stabilization? To what extent are hybrid genomes shaped by selection for compatibility? Is there a tendency for reversal towards one parent species during genome stabilization in homoploid hybrids? Does donor ancestry typically remain primarily in high recombination tracts c.f. or are there generally stable solutions with high contributions from both parent species across the genome c.f.? What are the relative effects of hybridization vs. polyploidization in generating new phenotypes during allopolyploid speciation? Does time to stabilization differ between homoploid and allopolyploid hybrid taxa? Are most orthologous genes lost over time in allopolyploid hybrids leaving only the ones where it is advantageous to have both as double copies c.f. ? Does genome size in allopolyploids vary predictably with taxon age or does this vary as in the Nicotiana? Hybrid genomes are important components of biodiversity and hybrid origin may spur adaptation. Future investigations into the properties of hybrid genomes will improve our understanding of the potential of hybridization to produce novel adaptive variation.

## Box: Detecting and studying hybridization with genomic tools

Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as STRUCTURE, ADMIXTURE or fineSTRUCTURE. These methods infer a user-specified number of genetic groups from the data and assign each individual to one or a mix of these groups. They can be applied to closely related taxa without having to preassign individuals to taxa and may thus be particularly useful in the study of closely related taxa or species complexes. However, uneven sampling of the parental taxa or different amounts of drift in the included taxa may lead to erroneous conclusions about evidence for hybridization. If genomic data of multiple species is available, phylogenetic methods may be better suited to identify introgression. Introgressive hybridization leads to gene trees that are discordant from the species tree, whereby introgressed individuals are phylogenetically closer to the source of introgression than to their non-introgressed conspecifics. Such discordant gene trees can also arise by chance through incomplete lineage sorting, particularly if the species compared are still young. Therefore, discordant gene trees are only evidence of introgression if a gene tree produced by excess allele sharing between the hybridizing taxa is strongly overrepresented compared to alternative discordant gene trees. An entire suite of methods have been developed to detect such excess allele sharing between hybridizing taxa, including Patterson’s D statstics or ABBA-BABA tests or f-statistics. Modified versions of these tests can be used to infer introgressed genomic regions, the direction of gene flow or the amount of gene flow. For datasets with a large number of taxa it may be difficult to compute all possible test of hybridization. In such cases, graph construction methods may be better suited. These methods reconstruct complex phylogenetic models with hybridization that best fit the genetic relationships among the sampled taxa and provide estimates for drift and introgression. Other phylogenetic network methods that account for incomplete lineage sorting and hybridization may also help. Methods based on linkage disequilibrium decay or methods inferring ancestry tracts can be used to date recent admixture or introgression events as over time ancestry tracts are continuously broken down by recombination. With increasing genome stabilization, individuals should vary less in local ancestry. Levels of genome stabilization can thus be assessed by computing the ancestry proportions (e.g. with fd) in genomic windows and testing if these correlate across individuals. Additionally, if hybridization is still ongoing, ancestry proportions should vary across individuals and in space. A different approach is to use demographic modelling to find the simplification of the evolutionary history of the studied taxa. Demographic modelling should only be applied to small sets of taxa because with increasing number of taxa model complexity increases and the number of model parameters such as timing, amounts and direction of gene flow, and population sizes and split times can quickly become too high. The fit of the demographic models to the data can be assessed with the site frequency spectrum or with summary statistics in an Approximate Bayesian Computation framework. It is also possible to gain more power by combining information from linkage disequilibrium decay patterns and the allele frequency spectrum.

## Glossary

* Ancestry block/introgression tracts - a region in the genome of a hybrid where all alleles are inherited from the same parent species.
* Allopolyploid species - a polyploid hybrid species where the two chromosome sets are derived from different parent species.
* Backcrossing - crossing of a hybrid with one of its parent species.
* Extrinsic incompatibilities - Environment-dependent reproductive barrier. For example, when trait combinations lead to reduced fitness in the hybrid offspring in specific environments.
* Genome stabilization - the process by which different ancestry blocks or introgression tracts become fixed within a hybrid species when hybridization between the hybrid taxon and its parent taxa has ceased.
* Hybrid - offspring resulting from interbreeding between two genetically distinct taxa, e.g. breeds or species.
* Hybrid genome - The genome of a hybrid individual, characterized by the presence of ancestry tracts from different species. In this review we focus mainly on hybrid genomes that result in separate lineages.
* Hybrid zone - geographical area in which two taxa (e.g. species or breeds) interbreed resulting in hybrid offspring.
* Homoploid hybridization - the formation of a hybrid with no change in chromosome number.
* Incomplete lineage sorting - when gene trees produced by single polymorphic sites or genetic regions deviate from the species level tree by chance. Such deviations between gene and species trees can arise from random fixation of alleles that were segregating in the ancestor. At each gene tree, taxa that fixed the same allele will show closer phylogenetic similarity than taxa that fixed different alleles.
* Introgressive hybridization - hybridization resulting in the transfer of a gene or genetic tract from one species into the gene pool of another species by repeated backcrossing.
* Intrinsic incompatibilities - environment-independent reproductive barriers.
* Linkage disequilibrium - the non-random association of alleles at different loci in a given population. The association can arise either through physical linkage for genes residing on the same chromosome, or through coinheritance of unlinked loci.
* Phenology - the study of periodical natural phenomena such as flowering time and bird migration and how these are influenced by season and climatic conditions.
* Polyploid hybridization - the formation of a hybrid involving whole genome duplication.
* Postzygotic incompatibilities - reproductive barrier arising after zygote formation, including inviability and sterility.
* Post-mating barriers - Reproductive barriers that act after mating. These can include barriers that act after mating but before the zygote is formed (Post-mating, pre-zygotic barriers).
* Pre-mating barriers - Factors that make individuals more likely to mate with members of their own taxon than of another taxon or prevent mating between the taxa. Examples include sexual traits and preferences that differ between the two taxa, mechanical mismatch during copulation, or mating at different times or in different habitats.
* Prezygotic incompatibilities - reproductive barrier acting before fertilization. For example, pollinator isolation, mechanical barriers preventing mating, and sperm/ovule incompatibilities that prevent fertilization.
* Reproductive isolation - the presence of barriers to successful crossbreeding. Barriers can be classified in a number of ways depending on their timing and mechanism. For example, barriers can be classified depending whether they act before zygote formation (prezygotic; e.g. pollinator isolation) or after zygote formation (postzygotic; e.g. hybrid inviability). They can also be classified by whether they act in the form of intrinsic barriers reducing viability or fertility in hybrid offspring or extrinsic barriers where hybrid offspring are ecologically less fit than the parents and selected against.
* Recombination rate - Recombination is a process during meiosis or mitosis by which pieces of homologous chromosomes are broken and recombined to new combinations. The frequency or rate of such recombination varies across the genome.
* Recombinational hybrid speciation - the process by which a hybrid population develops reproductive isolation from the parent species through sorting of incompatibilities leading to combinations that are incompatible with both parent species but compatible within the hybrid taxon.
* Transgressive phenotypes - extreme phenotypes in hybrids, exceeding trait values of both parent lineages.

## Wikipedia links

* Hybrid
* Polyploidy
* Haldane's rule
* Recombination

# References

* 1 2 3 4 5 6 7 Abbott, R.; Albach, D.; Ansell, S.; Arntzen, J. W.; Baird, S. J. E.; Bierne, N.; Boughman, J.; Brelsford, A.; Buerkle, C. A. (2013), "Hybridization and speciation", Journal of Evolutionary Biology, 26 (2): 229–246, doi:10.1111/j.1420-9101.2012.02599.x
* ↑ Fisher, Ronald Aylmer (1930), The genetical theory of natural selection., Oxford: Clarendon Press, doi:10.5962/bhl.title.27468 {{citation}}: Text "book" ignored (help)
* ↑ Mayr, Ernst (1963), Animal Species and Evolution:, Cambridge, MA and London, England: Harvard University Press, doi:10.4159/harvard.9780674865327, ISBN 9780674865327 {{citation}}: Text "book" ignored (help)
* 1 2 Stebbins, G. Ledyard (1959), "The Role of Hybridization in Evolution", Proceedings of the American Philosophical Society, 103 (2): 231–251, ISSN 0003-049X
* ↑ Anderson, E.; Stebbins, G. L. (1954), "Hybridization as an evolutionary stimulus", Evolution, 8 (4): 378–388, doi:10.1111/j.1558-5646.1954.tb01504.x, ISSN 0014-3820
* ↑ Arnold, Michael L. (1997), Natural Hybridization and Evolution., Cary: Oxford University Press, ISBN 9780195356687, OCLC 960164734 {{citation}}: Text "book" ignored (help)
* ↑ Mallet, James; Besansky, Nora; Hahn, Matthew W. (2016), "How reticulated are species?", BioEssays, 38 (2): 140–149, doi:10.1002/bies.201500149, PMC 4813508, PMID 26709836{{citation}}: CS1 maint: PMC format (link)
* 1 2 Lamichhaney, Sangeet; Han, Fan; Webster, Matthew T.; Andersson, Leif; Grant, B. Rosemary; Grant, Peter R. (2018), "Rapid hybrid speciation in Darwin's finches", Science, 359 (6372): 224–228, doi:10.1126/science.aao4593, ISSN 0036-8075
* ↑ Meier, Joana I.; Marques, David A.; Mwaiko, Salome; Wagner, Catherine E.; Excoffier, Laurent; Seehausen, Ole (2017), "Ancient hybridization fuels rapid cichlid fish adaptive radiations", Nature Communications, 8 (1), doi:10.1038/ncomms14363, ISSN 2041-1723, PMC 5309898, PMID 28186104{{citation}}: CS1 maint: PMC format (link)
* 1 2 Mavárez, Jesús; Salazar, Camilo A.; Bermingham, Eldredge; Salcedo, Christian; Jiggins, Chris D.; Linares, Mauricio (2006), "Speciation by hybridization in Heliconius butterflies", Nature, 441 (7095): 868–871, doi:10.1038/nature04738, ISSN 0028-0836
* 1 2 Salazar, Camilo; Baxter, Simon W.; Pardo-Diaz, Carolina; Wu, Grace; Surridge, Alison; Linares, Mauricio; Bermingham, Eldredge; Jiggins, Chris D. (2010), Walsh, Bruce (ed.), "Genetic Evidence for Hybrid Trait Speciation in Heliconius Butterflies", PLoS Genetics, 6 (4): e1000930, doi:10.1371/journal.pgen.1000930, ISSN 1553-7404, PMC 2861694, PMID 20442862{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 Melo, Maria C.; Salazar, Camilo; Jiggins, Chris D.; Linares, Mauricio (2009), "Assortative mating preferences among hybrids offers a route to hybrid speciation", Evolution, 63 (6): 1660–1665, doi:10.1111/j.1558-5646.2009.00633.x
* ↑ Tarweeds & silverswords : evolution of the Madiinae (Asteraceae), Carlquist, Sherwin John, 1930-, Baldwin, Bruce G., 1957-, Carr, Gerald D., St. Louis: Missouri Botanical Garden Press, 2003, ISBN 1930723202, OCLC 52892451 {{citation}}: Text "book" ignored (help)CS1 maint: others (link)
* 1 2 Wolf, Diana E.; Takebayashi, Naoki; Rieseberg, Loren H. (2001), "Predicting the Risk of Extinction through Hybridization", Conservation Biology, 15 (4): 1039–1053, doi:10.1046/j.1523-1739.2001.0150041039.x, ISSN 0888-8892
* ↑ Prentis, P. J.; White, E. M.; Radford, I. J.; Lowe, A. J.; Clarke, A. R. (2007), "Can hybridization cause local extinction: a case for demographic swamping of the Australian native Senecio pinnatifolius by the invasive Senecio madagascariensis?", New Phytologist, 176 (4): 902–912, doi:10.1111/j.1469-8137.2007.02217.x, ISSN 0028-646X
* ↑ Servedio, Maria R.; Noor, Mohamed A.F. (2003), "The Role of Reinforcement in Speciation: Theory and Data", Annual Review of Ecology, Evolution, and Systematics, 34 (1): 339–364, doi:10.1146/annurev.ecolsys.34.011802.132412, ISSN 1543-592X
* ↑ Rhymer, Judith M.; Simberloff, Daniel (1996), "EXTINCTION BY HYBRIDIZATION AND INTROGRESSION", Annual Review of Ecology and Systematics, 27 (1): 83–109, doi:10.1146/annurev.ecolsys.27.1.83, ISSN 0066-4162
* ↑ Seehausen, Ole (2006), "Conservation: Losing Biodiversity by Reverse Speciation", Current Biology, 16 (9): R334–R337, doi:10.1016/j.cub.2006.03.080
* 1 2 Thompson, John D. (1994), "Harrison, R. G. (ed.). Hybrid Zones and the Evolutionary Process. Oxford University Press, Oxford. 364 pp. Price f45.00. ISBN: 0-19-506917-X.", Journal of Evolutionary Biology, 7 (5): 631–634, doi:10.1046/j.1420-9101.1994.7050631.x, ISSN 1010-061X
* 1 2 The Heliconius Genome Consortium (2012), "Butterfly genome reveals promiscuous exchange of mimicry adaptations among species", Nature, 487 (7405): 94–98, doi:10.1038/nature11041, ISSN 0028-0836, PMC 3398145, PMID 22722851{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 4 5 Hanemaaijer, Mark J.; Collier, Travis C.; Chang, Allison; Shott, Chloe C.; Houston, Parker D.; Schmidt, Hanno; Main, Bradley J.; Cornel, Anthony J.; Lee, Yoosook (2018), "The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population", Molecular Ecology, 27 (24): 4978–4990, doi:10.1111/mec.14947
* 1 2 Coyne, Jerry A.; Orr, H. Allen (2004), Speciation, Sunderland: Sinauer Associates, ISBN 0878930914, OCLC 55078441 {{citation}}: Text "book" ignored (help)
* ↑ Price, Trevor D.; Bouvier, Michelle M. (2002), "The evolution of F1 postzygotic incompatibilities in birds", Evolution, 56 (10): 2083, doi:10.1554/0014-3820(2002)056[2083:teofpi]2.0.co;2, ISSN 0014-3820
* ↑ Stelkens, Rike B.; Young, Kyle A.; Seehausen, Ole (2010), "The accumulation of reproductive incompatibilities in African cichlid fish", Evolution, 64 (3): 617–633, doi:10.1111/j.1558-5646.2009.00849.x
* ↑ Rebernig, Carolin A.; Lafon-Placette, Clément; Hatorangan, Marcelinus R.; Slotte, Tanja; Köhler, Claudia (2015), Bomblies, Kirsten (ed.), "Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm", PLOS Genetics, 11 (6): e1005295, doi:10.1371/journal.pgen.1005295, ISSN 1553-7404, PMC 4472357, PMID 26086217{{citation}}: CS1 maint: PMC format (link)
* ↑ Pritchard, V. L.; Knutson, V. L.; Lee, M.; Zieba, J.; Edmands, S. (2013), "Fitness and morphological outcomes of many generations of hybridization in the copepod Tigriopus californicus", Journal of Evolutionary Biology, 26 (2): 416–433, doi:10.1111/jeb.12060
* ↑ Rieseberg, Loren H; Archer, Margaret A; Wayne, Robert K (1999), "Transgressive segregation, adaptation and speciation", Heredity, 83 (4): 363–372, doi:10.1038/sj.hdy.6886170, ISSN 0018-067X
* 1 2 3 Burke, John M.; Arnold, Michael L. (2001), "Genetics and the Fitness of Hybrids", Annual Review of Genetics, 35 (1): 31–52, doi:10.1146/annurev.genet.35.102401.085719, ISSN 0066-4197
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* 1 2 Vallejo‐Marín, Mario; Hiscock, Simon J. (2016), "Hybridization and hybrid speciation under global change", New Phytologist, 211 (4): 1170–1187, doi:10.1111/nph.14004, ISSN 0028-646X
* ↑ Barton, Nick; Bengtsson, Bengt Olle (1986), "The barrier to genetic exchange between hybridising populations", Heredity, 57 (3): 357–376, doi:10.1038/hdy.1986.135, ISSN 0018-067X
* ↑ Demon, Inez; Haccou, Patsy; van den Bosch, Frank (2007), "Introgression of resistance genes between populations: A model study of insecticide resistance in Bemisia tabaci", Theoretical Population Biology, 72 (2): 292–304, doi:10.1016/j.tpb.2007.06.005
* ↑ Uecker, Hildegard; Setter, Derek; Hermisson, Joachim (2015), "Adaptive gene introgression after secondary contact", Journal of Mathematical Biology, 70 (7): 1523–1580, doi:10.1007/s00285-014-0802-y, ISSN 0303-6812, PMC 4426140, PMID 24992884{{citation}}: CS1 maint: PMC format (link)
* 1 2 Pardo-Diaz, Carolina; Salazar, Camilo; Baxter, Simon W.; Merot, Claire; Figueiredo-Ready, Wilsea; Joron, Mathieu; McMillan, W. Owen; Jiggins, Chris D. (2012), R. Kronforst, Marcus (ed.), "Adaptive Introgression across Species Boundaries in Heliconius Butterflies", PLoS Genetics, 8 (6): e1002752, doi:10.1371/journal.pgen.1002752, ISSN 1553-7404, PMC 3380824, PMID 22737081{{citation}}: CS1 maint: PMC format (link)
* ↑ Arnold, Brian J.; Lahner, Brett; DaCosta, Jeffrey M.; Weisman, Caroline M.; Hollister, Jesse D.; Salt, David E.; Bomblies, Kirsten; Yant, Levi (2016), "Borrowed alleles and convergence in serpentine adaptation", Proceedings of the National Academy of Sciences, 113 (29): 8320–8325, doi:10.1073/pnas.1600405113, ISSN 0027-8424, PMC 4961121, PMID 27357660{{citation}}: CS1 maint: PMC format (link)
* ↑ Racimo, Fernando; Sankararaman, Sriram; Nielsen, Rasmus; Huerta-Sánchez, Emilia (2015), "Evidence for archaic adaptive introgression in humans", Nature Reviews Genetics, 16 (6): 359–371, doi:10.1038/nrg3936, ISSN 1471-0056, PMC 4478293, PMID 25963373{{citation}}: CS1 maint: PMC format (link)
* ↑ Kronforst, M. R.; Papa, R. (2015), "The Functional Basis of Wing Patterning in Heliconius Butterflies: The Molecules Behind Mimicry", Genetics, 200 (1): 1–19, doi:10.1534/genetics.114.172387, ISSN 0016-6731, PMC 4423356, PMID 25953905{{citation}}: CS1 maint: PMC format (link)
* ↑ Mérot, C.; Salazar, C.; Merrill, R. M.; Jiggins, C. D.; Joron, M. (2017), "What shapes the continuum of reproductive isolation? Lessons from Heliconius butterflies", Proceedings of the Royal Society B: Biological Sciences, 284 (1856): 20170335, doi:10.1098/rspb.2017.0335, ISSN 0962-8452, PMC 5474069, PMID 28592669{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 Schumer, Molly; Rosenthal, Gil G.; Andolfatto, Peter (2014), "How common is homoploid hybrid speciation", Evolution, 68 (6): 1553–1560, doi:10.1111/evo.12399
* 1 2 Nieto Feliner, G; Álvarez, I; Fuertes-Aguilar, J; Heuertz, M; Marques, I; Moharrek, F; Piñeiro, R; Riina, R; Rosselló, J A (2017), "Is homoploid hybrid speciation that rare? An empiricist's view", Heredity, 118 (6): 513–516, doi:10.1038/hdy.2017.7, ISSN 0018-067X, PMC 5436029, PMID 28295029{{citation}}: CS1 maint: PMC format (link)
* 1 2 Rieseberg, L. H. (2003), "Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization", Science, 301 (5637): 1211–1216, doi:10.1126/science.1086949, ISSN 0036-8075
* ↑ Grant, Verne. (1981), Plant speciation (2nd ed ed.), New York: Columbia University Press, ISBN 0231051123, OCLC 7552165 {{citation}}: |edition= has extra text (help); Text "book" ignored (help)
* 1 2 3 4 5 Schumer, Molly; Xu, Chenling; Powell, Daniel L.; Durvasula, Arun; Skov, Laurits; Holland, Chris; Blazier, John C.; Sankararaman, Sriram; Andolfatto, Peter (2018), "Natural selection interacts with recombination to shape the evolution of hybrid genomes", Science, 360 (6389): 656–660, doi:10.1126/science.aar3684, ISSN 0036-8075, PMC 6069607, PMID 29674434{{citation}}: CS1 maint: PMC format (link)
* 1 2 Runemark, Anna; Trier, Cassandra N.; Eroukhmanoff, Fabrice; Hermansen, Jo S.; Matschiner, Michael; Ravinet, Mark; Elgvin, Tore O.; Sætre, Glenn-Peter (2018), "Variation and constraints in hybrid genome formation", Nature Ecology & Evolution, 2 (3): 549–556, doi:10.1038/s41559-017-0437-7, ISSN 2397-334X
* 1 2 3 4 5 Buerkle, C. Alex; Rieseberg, Loren H. (2008), "The rate of genome stabilization in homoploid hybrid species", Evolution, 62 (2): 266–275, doi:10.1111/j.1558-5646.2007.00267.x, ISSN 0014-3820, PMC 2442919, PMID 18039323{{citation}}: CS1 maint: PMC format (link)
* ↑ Ungerer, M. C.; Baird, S. J. E.; Pan, J.; Rieseberg, L. H. (1998), "Rapid hybrid speciation in wild sunflowers", Proceedings of the National Academy of Sciences, 95 (20): 11757–11762, doi:10.1073/pnas.95.20.11757, ISSN 0027-8424, PMC 21713, PMID 9751738{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 Lai, Zhao; Nakazato, Takuya; Salmaso, Marzia; Burke, John M.; Tang, Shunxue; Knapp, Steven J.; Rieseberg, Loren H. (2005), "Extensive Chromosomal Repatterning and the Evolution of Sterility Barriers in Hybrid Sunflower Species", Genetics, 171 (1): 291–303, doi:10.1534/genetics.105.042242, ISSN 0016-6731, PMC 1456521, PMID 16183908{{citation}}: CS1 maint: PMC format (link)
* 1 2 Elgvin, Tore O.; Trier, Cassandra N.; Tørresen, Ole K.; Hagen, Ingerid J.; Lien, Sigbjørn; Nederbragt, Alexander J.; Ravinet, Mark; Jensen, Henrik; Sætre, Glenn-Peter (2017), "The genomic mosaicism of hybrid speciation", Science Advances, 3 (6): e1602996, doi:10.1126/sciadv.1602996, ISSN 2375-2548, PMC 5470830, PMID 28630911{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 4 5 Runemark, Anna; Trier, Cassandra N.; Eroukhmanoff, Fabrice; Hermansen, Jo S.; Matschiner, Michael; Ravinet, Mark; Elgvin, Tore O.; Sætre, Glenn-Peter (2018), "Variation and constraints in hybrid genome formation", Nature Ecology & Evolution, 2 (3): 549–556, doi:10.1038/s41559-017-0437-7, ISSN 2397-334X
* 1 2 Otto, Sarah P; Whitton, Jeannette (2000), "Polyploid Incidence and Evolution", Annual Review of Genetics, 34 (1): 401–437, doi:10.1146/annurev.genet.34.1.401, ISSN 0066-4197
* ↑ Abbott, Richard J; Rieseberg, Loren H (2012), John Wiley & Sons, Ltd (ed.), "Hybrid Speciation", eLS, John Wiley & Sons, Ltd, doi:10.1002/9780470015902.a0001753.pub2, ISBN 9780470016176
* 1 2 Coyne, Jerry A (1989), "Mutation rates in hybrids between sibling species of Drosophila", Heredity, 63 (2): 155–162, doi:10.1038/hdy.1989.87, ISSN 0018-067X
* ↑ Chase, Mark W; Paun, Ovidiu; Fay, Michael F (2010), "Hybridization and speciation in angiosperms: arole for pollinator shifts?", Journal of Biology, 9 (3): 21, doi:10.1186/jbiol231, ISSN 1475-4924
* ↑ Grant, Verne (1949), "Pollination systems as isolating mechanisms in angiosperms", Evolution, 3 (1): 82–97, doi:10.1111/j.1558-5646.1949.tb00007.x
* ↑ Segraves, K. A.; Thompson, J. N. (1999), "Plant polyploidy and pollination: floral traits and insect visits to diploid and tetraploid Heuchera grossulariifolia", Evolution, 53 (4): 1114–1127, doi:10.1111/j.1558-5646.1999.tb04526.x
* ↑ Moe, Annika M.; Weiblen, George D. (2012), "Pollinator-mediated reproductive isolation among dioecious fig species (Ficus, Moraceae)", Evolution, 66 (12): 3710–3721, doi:10.1111/j.1558-5646.2012.01727.x
* 1 2 Lowe, A J; Abbott, R J (2004), "Reproductive isolation of a new hybrid species, Senecio eboracensis Abbott & Lowe (Asteraceae)", Heredity, 92 (5): 386–395, doi:10.1038/sj.hdy.6800432, ISSN 0018-067X
* ↑ Selz, O. M.; Thommen, R.; Maan, M. E.; Seehausen, O. (2014), "Behavioural isolation may facilitate homoploid hybrid speciation in cichlid fish", Journal of Evolutionary Biology, 27 (2): 275–289, doi:10.1111/jeb.12287
* 1 2 Schwarzbach, Andrea E.; Donovan, Lisa A.; Rieseberg, Loren H. (2001), "Transgressive character expression in a hybrid sunflower species", American Journal of Botany, 88 (2): 270–277, doi:10.2307/2657018, ISSN 0002-9122
* ↑ Mameli, Giulia; López-Alvarado, Javier; Farris, Emmanuele; Susanna, Alfonso; Filigheddu, Rossella; Garcia-Jacas, Núria (2014), "The role of parental and hybrid species in multiple introgression events: evidence of homoploid hybrid speciation in Centaurea (Cardueae, Asteraceae): Introgression in Centaurea", Botanical Journal of the Linnean Society, 175 (3): 453–467, doi:10.1111/boj.12177
* ↑ Xie, X.; Michel, A. P.; Schwarz, D.; Rull, J.; Velez, S.; Forbes, A. A.; Aluja, M.; Feder, J. L. (2008), "Radiation and divergence in the Rhagoletis Pomonella species complex: inferences from DNA sequence data", Journal of Evolutionary Biology, 21 (3): 900–913, doi:10.1111/j.1420-9101.2008.01507.x, ISSN 1010-061X
* ↑ Feder, J. L.; Xie, X.; Rull, J.; Velez, S.; Forbes, A.; Leung, B.; Dambroski, H.; Filchak, K. E.; Aluja, M. (2005), "Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis", Proceedings of the National Academy of Sciences, 102 (Supplement 1): 6573–6580, doi:10.1073/pnas.0502099102, ISSN 0027-8424, PMC 1131876, PMID 15851672{{citation}}: CS1 maint: PMC format (link)
* ↑ Schumer, Molly; Powell, Daniel L.; Delclós, Pablo J.; Squire, Mattie; Cui, Rongfeng; Andolfatto, Peter; Rosenthal, Gil G. (2017), "Assortative mating and persistent reproductive isolation in hybrids", Proceedings of the National Academy of Sciences, 114 (41): 10936–10941, doi:10.1073/pnas.1711238114, ISSN 0027-8424, PMC 5642718, PMID 28973863{{citation}}: CS1 maint: PMC format (link)
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* ↑ Blanckaert, Alexandre; Bank, Claudia (2018), Zhang, Jianzhi (ed.), "In search of the Goldilocks zone for hybrid speciation", PLOS Genetics, 14 (9): e1007613, doi:10.1371/journal.pgen.1007613, ISSN 1553-7404, PMC 6145587, PMID 30192761{{citation}}: CS1 maint: PMC format (link)
* ↑ Schumer, Molly; Cui, Rongfeng; Rosenthal, Gil G.; Andolfatto, Peter (2015), Payseur, Bret A. (ed.), "Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities", PLOS Genetics, 11 (3): e1005041, doi:10.1371/journal.pgen.1005041, ISSN 1553-7404, PMC 4359097, PMID 25768654{{citation}}: CS1 maint: PMC format (link)
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* ↑ Rieseberg, L. H.; Sinervo, B.; Linder, C. R.; Ungerer, M. C.; Arias, D. M. (1996), "Role of Gene Interactions in Hybrid Speciation: Evidence from Ancient and Experimental Hybrids", Science, 272 (5262): 741–745, doi:10.1126/science.272.5262.741, ISSN 0036-8075
* ↑ Stukenbrock, E. H.; Christiansen, F. B.; Hansen, T. T.; Dutheil, J. Y.; Schierup, M. H. (2012), "Fusion of two divergent fungal individuals led to the recent emergence of a unique widespread pathogen species", Proceedings of the National Academy of Sciences, 109 (27): 10954–10959, doi:10.1073/pnas.1201403109, ISSN 0027-8424, PMC 3390827, PMID 22711811{{citation}}: CS1 maint: PMC format (link)
* 1 2 3 Schumer, Molly; Brandvain, Yaniv (2016), "Determining epistatic selection in admixed populations", Molecular Ecology, 25 (11): 2577–2591, doi:10.1111/mec.13641
* ↑ Sankararaman, Sriram; Mallick, Swapan; Dannemann, Michael; Prüfer, Kay; Kelso, Janet; Pääbo, Svante; Patterson, Nick; Reich, David (2014), "The genomic landscape of Neanderthal ancestry in present-day humans", Nature, 507 (7492): 354–357, doi:10.1038/nature12961, ISSN 0028-0836, PMC 4072735, PMID 24476815{{citation}}: CS1 maint: PMC format (link)
* ↑ Eroukhmanoff, Fabrice; Bailey, Richard I.; Elgvin, Tore O.; Hermansen, Jo S.; Runemark, Anna R.; Trier, Cassandra N.; Sætre, Glenn-Peter (2017), "Resolution of conflict between parental genomes in a hybrid species", bioRxiv, doi:10.1101/102970
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* 1 2 Barton, Nicholas H. (2018), "The consequences of an introgression event", Molecular Ecology, 27 (24): 4973–4975, doi:10.1111/mec.14950
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* ↑ Brandvain, Yaniv; Kenney, Amanda M.; Flagel, Lex; Coop, Graham; Sweigart, Andrea L. (2014), Jiggins, Chris D. (ed.), "Speciation and Introgression between Mimulus nasutus and Mimulus guttatus", PLoS Genetics, 10 (6): e1004410, doi:10.1371/journal.pgen.1004410, ISSN 1553-7404, PMC 4072524, PMID 24967630{{citation}}: CS1 maint: PMC format (link)
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* ↑ Schumer, Molly; Cui, Rongfeng; Powell, Daniel L; Dresner, Rebecca; Rosenthal, Gil G; Andolfatto, Peter (2014), "High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species", eLife, 3, doi:10.7554/eLife.02535, ISSN 2050-084X, PMC 4080447, PMID 24898754{{citation}}: CS1 maint: PMC format (link)
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* ↑ Giordano, Luana; Sillo, Fabiano; Garbelotto, Matteo; Gonthier, Paolo (2018), "Mitonuclear interactions may contribute to fitness of fungal hybrids", Scientific Reports, 8 (1), doi:10.1038/s41598-018-19922-w, ISSN 2045-2322, PMC 5786003, PMID 29374209{{citation}}: CS1 maint: PMC format (link)
* ↑ Case, Andrea L.; Finseth, Findley R.; Barr, Camille M.; Fishman, Lila (2016), "Selfish evolution of cytonuclear hybrid incompatibility in Mimulus", Proceedings of the Royal Society B: Biological Sciences, 283 (1838): 20161493, doi:10.1098/rspb.2016.1493, ISSN 0962-8452, PMC 5031664, PMID 27629037{{citation}}: CS1 maint: PMC format (link)
* ↑ David, Wendi M.; Mitchell, David L.; Walter, Ronald B. (2004), "DNA repair in hybrid fish of the genus Xiphophorus", Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 138 (3): 301–309, doi:10.1016/j.cca.2004.07.006
* ↑ Ávila, Victoria; Chavarrías, David; Sánchez, Enrique; Manrique, Antonio; López-Fanjul, Carlos; García-Dorado, Aurora (2006), "Increase of the Spontaneous Mutation Rate in a Long-Term Experiment With Drosophila melanogaster", Genetics, 173 (1): 267–277, doi:10.1534/genetics.106.056200, ISSN 0016-6731, PMC 1461422, PMID 16547099{{citation}}: CS1 maint: PMC format (link)
* ↑ Bashir, Tufail; Sailer, Christian; Gerber, Florian; Loganathan, Nitin; Bhoopalan, Hemadev; Eichenberger, Christof; Grossniklaus, Ueli; Baskar, Ramamurthy (2014), "Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis", Plant Physiology, 165 (1): 424–437, doi:10.1104/pp.114.238451, ISSN 0032-0889, PMC 4012600, PMID 24664208{{citation}}: CS1 maint: PMC format (link)
* ↑ Dennenmoser, Stefan; Sedlazeck, Fritz J.; Iwaszkiewicz, Elzbieta; Li, Xiang-Yi; Altmüller, Janine; Nolte, Arne W. (2017), "Copy number increases of transposable elements and protein-coding genes in an invasive fish of hybrid origin", Molecular Ecology, 26 (18): 4712–4724, doi:10.1111/mec.14134, PMC 5638112, PMID 28390096{{citation}}: CS1 maint: PMC format (link)
* ↑ Dion-Côté, Anne-Marie; Renaut, Sébastien; Normandeau, Eric; Bernatchez, Louis (2014), "RNA-seq Reveals Transcriptomic Shock Involving Transposable Elements Reactivation in Hybrids of Young Lake Whitefish Species", Molecular Biology and Evolution, 31 (5): 1188–1199, doi:10.1093/molbev/msu069, ISSN 1537-1719
* ↑ Senerchia, Natacha; Felber, François; Parisod, Christian (2015), "Genome reorganization in F1 hybrids uncovers the role of retrotransposons in reproductive isolation", Proceedings of the Royal Society B: Biological Sciences, 282 (1804): 20142874, doi:10.1098/rspb.2014.2874, ISSN 0962-8452, PMC 4375867, PMID 25716787{{citation}}: CS1 maint: PMC format (link)
* ↑ Ostberg, Carl O; Hauser, Lorenz; Pritchard, Victoria L; Garza, John C; Naish, Kerry A (2013), "Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and rainbow trout (O. mykiss)", BMC Genomics, 14 (1): 570, doi:10.1186/1471-2164-14-570, ISSN 1471-2164, PMC 3765842, PMID 23968234{{citation}}: CS1 maint: PMC format (link)
* ↑ Hirai, Hirohisa; Hirai, Yuriko; Morimoto, Mayumi; Kaneko, Akihisa; Kamanaka, Yoshiro; Koga, Akihiko (2017), "Night Monkey Hybrids Exhibit De Novo Genomic and Karyotypic Alterations: The First Such Case in Primates", Genome Biology and Evolution, 9 (4): 945–955, doi:10.1093/gbe/evx058, ISSN 1759-6653, PMC 5388293, PMID 28369492{{citation}}: CS1 maint: PMC format (link)
* ↑ Barkan, A.; Martienssen, R. A. (1991), "Inactivation of maize transposon Mu suppresses a mutant phenotype by activating an outward-reading promoter near the end of Mu1.", Proceedings of the National Academy of Sciences, 88 (8): 3502–3506, doi:10.1073/pnas.88.8.3502, ISSN 0027-8424
* ↑ Raizada, Manish N.; Benito, Maria-Ines; Walbot, Virginia (2008), "The MuDR transposon terminal inverted repeat contains a complex plant promoter directing distinct somatic and germinal programs: Transposon promoter expression pattern", The Plant Journal, 25 (1): 79–91, doi:10.1111/j.1365-313X.2001.00939.x
* ↑ Lim, Kar Yoong; Matyasek, Roman; Kovarik, Ales; Leitch, Andrew R. (2004), "Genome evolution in allotetraploid Nicotiana", Biological Journal of the Linnean Society, 82 (4): 599–606, doi:10.1111/j.1095-8312.2004.00344.x
* 1 2 Baack, Eric J.; Whitney, Kenneth D.; Rieseberg, Loren H. (2005), "Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species", New Phytologist, 167 (2): 623–630, doi:10.1111/j.1469-8137.2005.01433.x
* 1 2 Leitch, I. J.; Hanson, L.; Lim, K. Y.; Kovarik, A.; Chase, M. W.; Clarkson, J. J.; Leitch, A. R. (2008), "The Ups and Downs of Genome Size Evolution in Polyploid Species of Nicotiana (Solanaceae)", Annals of Botany, 101 (6): 805–814, doi:10.1093/aob/mcm326, ISSN 0305-7364, PMC 2710205, PMID 18222910{{citation}}: CS1 maint: PMC format (link)
* ↑ Wolfe, Kenneth H. (2001), "Yesterday's polyploids and the mystery of diploidization", Nature Reviews Genetics, 2 (5): 333–341, doi:10.1038/35072009, ISSN 1471-0056
* 1 2 3 Freeling, Michael; Scanlon, Michael J; Fowler, John E (2015), "Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences", Current Opinion in Genetics & Development, 35: 110–118, doi:10.1016/j.gde.2015.11.002
* 1 2 Sankoff, David; Zheng, Chunfang; Zhu, Qian (2010), "The collapse of gene complement following whole genome duplication", BMC Genomics, 11 (1): 313, doi:10.1186/1471-2164-11-313, ISSN 1471-2164, PMC 2896955, PMID 20482863{{citation}}: CS1 maint: PMC format (link)
* 1 2 Edger, Patrick P.; Poorten, Thomas J.; VanBuren, Robert; Hardigan, Michael A.; Colle, Marivi; McKain, Michael R.; Smith, Ronald D.; Teresi, Scott J.; Nelson, Andrew D. L. (2019), "Origin and evolution of the octoploid strawberry genome", Nature Genetics, 51 (3): 541–547, doi:10.1038/s41588-019-0356-4, ISSN 1061-4036
* 1 2 Edger, Patrick P.; Smith, Ronald; McKain, Michael R.; Cooley, Arielle M.; Vallejo-Marin, Mario; Yuan, Yaowu; Bewick, Adam J.; Ji, Lexiang; Platts, Adrian E. (2017), "Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower", The Plant Cell, 29 (9): 2150–2167, doi:10.1105/tpc.17.00010, ISSN 1040-4651, PMC 5635986, PMID 28814644{{citation}}: CS1 maint: PMC format (link)
* ↑ Xu, Chunming; Bai, Yan; Lin, Xiuyun; Zhao, Na; Hu, Lanjuan; Gong, Zhiyun; Wendel, Jonathan F.; Liu, Bao (2014), "Genome-Wide Disruption of Gene Expression in Allopolyploids but Not Hybrids of Rice Subspecies", Molecular Biology and Evolution, 31 (5): 1066–1076, doi:10.1093/molbev/msu085, ISSN 1537-1719, PMC 3995341, PMID 24577842{{citation}}: CS1 maint: PMC format (link)
* ↑ Renaut, S.; Nolte, A.W.; Bernatchez, L. (2009), "Gene Expression Divergence and Hybrid Misexpression between Lake Whitefish Species Pairs (Coregonus spp. Salmonidae)", Molecular Biology and Evolution, 26 (4): 925–936, doi:10.1093/molbev/msp017, ISSN 1537-1719
* ↑ Buggs, Richard J.A.; Zhang, Linjing; Miles, Nicholas; Tate, Jennifer A.; Gao, Lu; Wei, Wu; Schnable, Patrick S.; Barbazuk, W. Brad; Soltis, Pamela S. (2011), "Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant", Current Biology, 21 (7): 551–556, doi:10.1016/j.cub.2011.02.016 {{citation}}: no-break space character in |first4= at position 9 (help); no-break space character in |first7= at position 8 (help); no-break space character in |first8= at position 3 (help); no-break space character in |first9= at position 7 (help); no-break space character in |first= at position 8 (help)
* ↑ Ha, M.; Lu, J.; Tian, L.; Ramachandran, V.; Kasschau, K. D.; Chapman, E. J.; Carrington, J. C.; Chen, X.; Wang, X.-J. (2009), "Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids", Proceedings of the National Academy of Sciences, 106 (42): 17835–17840, doi:10.1073/pnas.0907003106, ISSN 0027-8424, PMC 2757398, PMID 19805056{{citation}}: CS1 maint: PMC format (link)
* ↑ Mallet, James (2005), "Hybridization as an invasion of the genome", Trends in Ecology & Evolution, 20 (5): 229–237, doi:10.1016/j.tree.2005.02.010
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* ↑ Rieseberg, Loren H. (2001), "Chromosomal rearrangements and speciation", Trends in Ecology & Evolution, 16 (7): 351–358, doi:10.1016/s0169-5347(01)02187-5, ISSN 0169-5347
* ↑ Levin, Donald A. (2012), "The long wait for hybrid sterility in flowering plants", New Phytologist, 196 (3): 666–670, doi:10.1111/j.1469-8137.2012.04309.x
* ↑ Haldane, J. B. S. (1922), "Sex ratio and unisexual sterility in hybrid animals", Journal of Genetics, 12 (2): 101–109, doi:10.1007/BF02983075, ISSN 0022-1333
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* ↑ Runemark, Anna; Eroukhmanoff, Fabrice; Nava-Bolaños, Angela; Hermansen, Jo S.; Meier, Joana I. (2018), "Hybridization, sex-specific genomic architecture and local adaptation", Philosophical Transactions of the Royal Society B: Biological Sciences, 373 (1757): 20170419, doi:10.1098/rstb.2017.0419, ISSN 0962-8436, PMC 6125728, PMID 30150218{{citation}}: CS1 maint: PMC format (link)
* ↑ Payseur, Bret A.; Rieseberg, Loren H. (2016), "A genomic perspective on hybridization and speciation", Molecular Ecology, 25 (11): 2337–2360, doi:10.1111/mec.13557, PMC 4915564, PMID 26836441{{citation}}: CS1 maint: PMC format (link)
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* ↑ Masly, John P; Presgraves, Daven C (2007), Barton, Nick H (ed.), "High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila", PLoS Biology, 5 (9): e243, doi:10.1371/journal.pbio.0050243, ISSN 1545-7885, PMC 1971125, PMID 17850182{{citation}}: CS1 maint: PMC format (link)
* ↑ Mank, J. E.; Hosken, D. J.; Wedell, N. (2014), "Conflict on the Sex Chromosomes: Cause, Effect, and Complexity", Cold Spring Harbor Perspectives in Biology, 6 (12): a017715–a017715, doi:10.1101/cshperspect.a017715, ISSN 1943-0264, PMC 4292157, PMID 25280765{{citation}}: CS1 maint: PMC format (link)
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* ↑ McCarthy, Eugene M; Asmussen, Marjorie A; Anderson, Wyatt W (1995), "A theoretical assessment of recombinational speciation", Heredity, 74 (5): 502–509, doi:10.1038/hdy.1995.71, ISSN 0018-067X
* ↑ Charlton, Nikki D.; Craven, Kelly D.; Afkhami, Michelle E.; Hall, Bradley A.; Ghimire, Sita R.; Young, Carolyn A. (2014), "Interspecific hybridization and bioactive alkaloid variation increases diversity in endophytic Epichloë species of Bromus laevipes", FEMS Microbiology Ecology, 90 (1): 276–289, doi:10.1111/1574-6941.12393
* ↑ Janko, Karel; Pačes, Jan; Wilkinson-Herbots, Hilde; Costa, Rui J.; Roslein, Jan; Drozd, Pavel; Iakovenko, Nataliia; Rídl, Jakub; Hroudová, Miluše (2018), "Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation", Molecular Ecology, 27 (1): 248–263, doi:10.1111/mec.14377
* ↑ Neaves, William B.; Baumann, Peter (2011), "Unisexual reproduction among vertebrates", Trends in Genetics, 27 (3): 81–88, doi:10.1016/j.tig.2010.12.002
* ↑ Brochmann, C.; Brysting, A. K.; Alsos, I. G.; Borgen, L.; Grundt, H. H.; Scheen, A.-C.; Elven, R. (2004), "Polyploidy in arctic plants", Biological Journal of the Linnean Society, 82 (4): 521–536, doi:10.1111/j.1095-8312.2004.00337.x
* ↑ Norris, Laura C.; Main, Bradley J.; Lee, Yoosook; Collier, Travis C.; Fofana, Abdrahamane; Cornel, Anthony J.; Lanzaro, Gregory C. (2015), "Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets", Proceedings of the National Academy of Sciences, 112 (3): 815–820, doi:10.1073/pnas.1418892112, ISSN 0027-8424, PMC 4311837, PMID 25561525{{citation}}: CS1 maint: PMC format (link)
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* ↑ Jiggins, Chris D; Salazar, Camilo; Linares, Mauricio; Mavarez, Jesus (2008), "Hybrid trait speciation and Heliconius butterflies", Philosophical Transactions of the Royal Society B: Biological Sciences, 363 (1506): 3047–3054, doi:10.1098/rstb.2008.0065, ISSN 0962-8436, PMC 2607310, PMID 18579480{{citation}}: CS1 maint: PMC format (link)
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* ↑ Jay, Paul; Whibley, Annabel; Frézal, Lise; Rodríguez de Cara, María Ángeles; Nowell, Reuben W.; Mallet, James; Dasmahapatra, Kanchon K.; Joron, Mathieu (2018), "Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion", Current Biology, 28 (11): 1839–1845.e3, doi:10.1016/j.cub.2018.04.072
* ↑ Yeaman, S. (2013), "Genomic rearrangements and the evolution of clusters of locally adaptive loci", Proceedings of the National Academy of Sciences, 110 (19): E1743–E1751, doi:10.1073/pnas.1219381110, ISSN 0027-8424, PMC 3651494, PMID 23610436{{citation}}: CS1 maint: PMC format (link)
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* ↑ Martin, Simon H.; Davey, John W.; Jiggins, Chris D. (2015), "Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci", Molecular Biology and Evolution, 32 (1): 244–257, doi:10.1093/molbev/msu269, ISSN 1537-1719, PMC 4271521, PMID 25246699{{citation}}: CS1 maint: PMC format (link)
* ↑ Pease, James B.; Hahn, Matthew W. (2015), "Detection and Polarization of Introgression in a Five-Taxon Phylogeny", Systematic Biology, 64 (4): 651–662, doi:10.1093/sysbio/syv023, ISSN 1076-836X
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* ↑ Pickrell, Joseph K.; Pritchard, Jonathan K. (2012), Tang, Hua (ed.), "Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data", PLoS Genetics, 8 (11): e1002967, doi:10.1371/journal.pgen.1002967, ISSN 1553-7404, PMC 3499260, PMID 23166502{{citation}}: CS1 maint: PMC format (link)
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* ↑ Lipson, Mark; Loh, Po-Ru; Levin, Alex; Reich, David; Patterson, Nick; Berger, Bonnie (2013), "Efficient Moment-Based Inference of Admixture Parameters and Sources of Gene Flow", Molecular Biology and Evolution, 30 (8): 1788–1802, doi:10.1093/molbev/mst099, ISSN 1537-1719, PMC 3708505, PMID 23709261{{citation}}: CS1 maint: PMC format (link)
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* ↑ Loh, Po-Ru; Lipson, Mark; Patterson, Nick; Moorjani, Priya; Pickrell, Joseph K.; Reich, David; Berger, Bonnie (2013), "Inferring Admixture Histories of Human Populations Using Linkage Disequilibrium", Genetics, 193 (4): 1233–1254, doi:10.1534/genetics.112.147330, ISSN 0016-6731
* ↑ Sankararaman, Sriram; Patterson, Nick; Li, Heng; Pääbo, Svante; Reich, David (2012), Akey, Joshua M. (ed.), "The Date of Interbreeding between Neandertals and Modern Humans", PLoS Genetics, 8 (10): e1002947, doi:10.1371/journal.pgen.1002947, ISSN 1553-7404, PMC 3464203, PMID 23055938{{citation}}: CS1 maint: PMC format (link)
* ↑ Pinho, Catarina; Hey, Jody (2010), "Divergence with Gene Flow: Models and Data", Annual Review of Ecology, Evolution, and Systematics, 41 (1): 215–230, doi:10.1146/annurev-ecolsys-102209-144644, ISSN 1543-592X
* ↑ Excoffier, Laurent; Dupanloup, Isabelle; Huerta-Sánchez, Emilia; Sousa, Vitor C.; Foll, Matthieu (2013), Akey, Joshua M. (ed.), "Robust Demographic Inference from Genomic and SNP Data", PLoS Genetics, 9 (10): e1003905, doi:10.1371/journal.pgen.1003905, ISSN 1553-7404, PMC 3812088, PMID 24204310{{citation}}: CS1 maint: PMC format (link)
* ↑ Gutenkunst, Ryan N.; Hernandez, Ryan D.; Williamson, Scott H.; Bustamante, Carlos D. (2009), McVean, Gil (ed.), "Inferring the Joint Demographic History of Multiple Populations from Multidimensional SNP Frequency Data", PLoS Genetics, 5 (10): e1000695, doi:10.1371/journal.pgen.1000695, ISSN 1553-7404, PMC 2760211, PMID 19851460{{citation}}: CS1 maint: PMC format (link)
* ↑ Beaumont, Mark A. (2010), "Approximate Bayesian Computation in Evolution and Ecology", Annual Review of Ecology, Evolution, and Systematics, 41 (1): 379–406, doi:10.1146/annurev-ecolsys-102209-144621
* ↑ Theunert, Christoph; Slatkin, Montgomery (2017), "Distinguishing Recent Admixture from Ancestral Population Structure", Genome Biology and Evolution, 9 (3): 427–437, doi:10.1093/gbe/evx018, ISSN 1759-6653, PMC 5381645, PMID 28186554{{citation}}: CS1 maint: PMC format (link)