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Insights from genomes into the evolutionary importance and prevalence of hybridization in nature

Abstract

Hybridization is an evolutionary phenomenon that has fascinated biologists for centuries. Prior to the advent of whole-genome sequencing, it was clear that hybridization had played a role in the evolutionary history of many extant taxa, particularly plants. The extent to which hybridization has contributed to the evolution of Earth’s biodiversity has, however, been the topic of much debate. Analyses of whole genomes are providing further insight into this evolutionary problem. Recent studies have documented ancient hybridization in a diverse array of taxa including mammals, birds, fish, fungi, and insects. Evidence for adaptive introgression is being documented in an increasing number of systems, though demonstrating the adaptive function of introgressed genomic regions remains difficult. And finally, several new homoploid hybrid speciation events have been reported. Here we review the current state of the field and specifically evaluate the additional insights gained from having access to whole-genome data and the challenges that remain with respect to understanding the evolutionary relevance and frequency of ancient hybridization, adaptive introgression, and hybrid speciation in nature.

Hybridization between species, subspecies, or lineages within species has long been viewed as a powerful tool for understanding evolutionary biology1,2,3,4. The study of hybridization has had two primary foci over the past century, one concerned with understanding species barriers and the other with the role of hybridization in generating novel gene combinations that selection can act on. The utility of using hybrid zones to understand the process of speciation (that is, to identify regions of the genome that likely are involved in the maintenance of reproductive isolation) is clear5,6,7 and has been the focus of hundreds of studies8,9,10,11,12. The crossing experiments that occur in natural hybrid zones would often be impossible to replicate in the lab, and the importance of studying hybridization in nature is hard to overstate.

The importance of hybridization in the processes of adaptation and speciation has, however, been rigorously debated in the literature, and a consensus that hybridization can, and often does, play a creative role in evolution13,14,15 has recently been forming. Importantly, the role that hybridization plays in the evolutionary history of different taxa is variable (there may be periods of introgression, hybrid speciation, and/or adaptive introgression), and the emphasis on certain outcomes of hybridization (for example, hybrid speciation) appear to be skewed in the literature16. Historically, botanists and zoologists approached this problem with different perspectives. The importance of hybridization in the evolution and diversification of plants is well-documented, and a creative role for hybridization in the evolution of plants has long been accepted17,18,19. Zoologists, on the other hand, have generally viewed hybridization as a useful tool for studying species barriers and reproductive isolation, but not as a source of genetic novelty that selection can act on20. There has been a significant shift in this view since the mid-1900s3,21, and many now see hybridization as a potentially creative force in evolution and adaptation for both plants and animals22,23.

It is becoming increasingly evident that hybridization, whether intermittent or ongoing, has played a major role in the evolutionary history of many taxa, including hominins24,25,26,27,28. For a long time, however, it has been difficult to fully understand the extent to which hybridization between closely related taxa has influenced their evolutionary histories. This is, in part, because researchers lacked the tools to dissect genomes at high resolution. Over the past decade, this landscape has rapidly changed, and whole genomes from most non-model taxa can now be sequenced at a relatively low cost. Studies that leverage genome-spanning data in their analyses are uncovering signatures of hybridization in taxa that were never really expected to have a history of hybridization29 and confirm previous hypotheses about the role of hybridization in diversification13,30,31,32.

In the era of high-throughput sequencing, scientists are better equipped than ever before to determine the extent to which hybridization has played a role in the evolution of life on Earth33. The tools are available and the methods are being developed to understand (1) the frequency of hybridization within evolutionary lineages34,35,36, particularly for taxa for which this was previously impossible37, (2) the context for hybridization between taxa (for example, hybrid zone structure and likelihood of introgression38,39, temporal variation9,40, and geographic variation41) and (3) what happens after hybridization occurs (how much of the genome remains after the initial hybridization event, and do reproductive barriers evolve between hybrid individuals and their parental taxa?)36,42,43.

Overall, it appears that outcomes of hybridization are more variable than was expected. Prior to high-throughput tools, geographically expansive, or temporally repeated, high-resolution investigations of hybridization in nature were difficult44. Recent studies have highlighted the important fact that hybridization is geographically variable36,41, and longitudinal studies that follow hybridization within populations over multiple generations36 have made it possible to see how reproductive isolation changes over time. The geographic context of hybridization along with the initial outcome of hybridization (the extent and time period of hybridization) are important, and it appears that generalizations from investigations of single or even a few hybrid zone transects should be avoided. Finally, many discoveries are being made in clades that have been difficult to study (fungi, for example) because morphology has typically been used to identify hybrids. Overall, during a short period of time, and thanks in large part to the rapid development of sequencing technology, researchers have gained many interesting and exciting insights into the role of hybridization in adaptation and speciation.

Progress in understanding the frequency of hybridization, the geographic and temporal variation in hybridization, and the consequences of hybridization is allowing us to begin to address other more complex questions about the ultimate consequences that hybridization has on species formation. What follows is a discussion of advances being made in understanding three aspects of hybridization—ancient hybridization, adaptive introgression, and hybrid speciation. When hybridization is not ongoing, it can be difficult to detect using traditional methods. For many taxa, however, it appears that ancient hybridization occurred at some point in their evolutionary history (Fig. 1). At the same time, linking introgression of gene regions and adaptive function is exceedingly difficult, yet recent studies have convincingly demonstrated that specific gene regions serve adaptive roles in the receiving lineages (Fig. 2). Finally, the hotly contested frequency and importance of homoploid hybrid speciation is being addressed in a diverse array of taxa. Several new studies shed additional light on this phenomenon, but few fulfill the criteria for homoploid hybrid speciation laid out in Schumer et al.16 (Fig. 3).

Fig. 1: There is increasing evidence for widespread ancient hybridization.
figure1

Melissa Hoyer (a,b); Croisy/Depositphotos.com (c, human skull); Creativemarc/Depositphotos.com (c, Neanderthal skull); iLexx/Depositphotos.com (d); vvoennyy/Depositphotos.com (e); Pierre Fidenci (f); David Toews (g); Ole Seehausen (h); chrupka/Depositphotos.com (map)

With increasing frequency, genome-spanning datasets are revealing that hybridization has played a role in the evolution of a diverse and globally distributed array of taxa. Though it is often hard to infer that ancient hybridization has played an adaptive role in the evolution of extant taxa, it certainly appears to be a common phenomenon. There are many taxa, including humans, for which there were no obvious reasons to suspect that hybridization played a role in their evolutionary history. Clarifying the importance of hybridization in the evolutionary history of these groups is an important next step in their study. Examples of hybridization are shown in ah. a, Hybridization between coyotes and gray wolves in north America51. b, Polar bear and brown bear hybridization during the last glacial maximum55. c, Human and Neanderthal hybridization following expansion of humans out of Africa24. d, Baker’s yeast hybridization before whole genome duplication34. e, Common bean hybridization with wild ancestors in South America77. f, Chimpanzee and bonobo hybridization53. g, Rampant ancient hybridization between extant and extinct elephantids29. h, Ancient hybridization between Congolese and Nile cichlid lineages appears to have led to the evolution of the Lake Victoria Super Flock of haplochromine cichlids30.

Fig. 2: Adaptive introgression is difficult to demonstrate.
figure2

ac, Many of the most convincing examples of adaptive introgression come from contemporary introgression events (a) or from traits with very clear adaptive function. For single loci of large effect (c), this is easier than for multigene traits (b). a, Liu et al.71 build on the work of Song et al.70, which reported introgression of genes involved in warfarin resistance from M. spretus to M. m. domesticus. Using 22 whole genomes, Liu et al.71 found evidence of three hybridization events, one ancient and two more recent, between M. spretus and M. m. domesticus. Importantly, they recovered the same introgressed region on chromosome 7 that contains Vkorc1, which is important for warfarin resistance, and find functional enrichment of olfactory receptors in introgressed regions. b, Suarez-Gonzalez et al.67 used whole-chromosome sequencing to investigate introgression and signals of selection of candidate genes involved in local adaptation from Populus balsamifera into Populus trichocarpa. Functional trait and gene expression analyses in a common garden setting reveal correlations between these genomic regions with traits that are adaptive at the northern range limit of P. trichocarpa, where the growing season is shorter (which leads to, for example, higher photosynthetic rates and faster growth). c, Jones et al.76 use a combination of whole-genome and whole-exome sequencing to demonstrate that cis-regulatory variation controls seasonal expression of the Agouti gene, which underlies seasonal coat color change in snowshoe hares. Their analyses indicate that the allele for brown coat color introgressed from the black-tailed jackrabbit and swept to high frequency in snowshoe hare populations in habitats with mild winters, where a brown coat color matches the winter background. d, The Heliconius Genome Consortium73 used whole-genome resequencing to document introgression between species, particularly of two genomic regions that control mimicry patterns between three species of Heliconius that are co-mimics. Heliconius butterflies are unpalatable to vertebrate predators and are considered a classic example of Mullerian mimicry: their warning color patterns enable multiple species to share the cost of predator education. Wing patterns are also important in mate selection.

Fig. 3: Hybrid speciation in nature appears to be rare.
figure3

K. Thalia Grant and Peter R. Grant (a); iLexx/Depositphotos.com (b)

An important component of documenting this form of speciation is providing evidence that hybridization itself led to reproductive isolation between the hybrid species and its parental taxa16. Although there are a growing number of reports of hybrid speciation in the literature, few systems have convincingly demonstrated the criteria outlined in Schumer et al.16. The two systems included here are recent examples of reported homoploid hybrid speciation that use whole genomes to clarify patterns of divergence and selection in hybrid lineages. Differentiating between homoploid hybrid speciation and introgression from ancient hybridization will be an important avenue of future research. a, Geospiza conirostris and Geospiza fortis hybridized to produce the Big Bird lineage87. b, Leducq et al.88,89 used whole-genome sequencing to investigate hybrid speciation in the budding yeast S. paradoxus.

Ancient hybridization is more common than we thought

A growing number of studies document ancient hybridization between lineages that may not have been expected to hybridize or more complex patterns of hybridization than would have been predicted (Fig. 1). These discoveries have the potential to help us understand the long-term consequences of hybridization. We consider hybridization ancient if there is no contemporary evidence of hybridization between taxa either because contemporary lineages are allopatric or one (or more) of the hybridizing lineages has gone extinct24,29,45. Two aspects of advances in sequencing technology are allowing rigorous study of ancient hybridization. First, scientists can now sequence whole genomes at a low cost, which provides the resolution necessary to detect small genomic blocks of hybrid origin24,35. With traditional panels of a handful of markers, this was not possible. New methods are being developed to exploit fine-scale variation in the length of ancestry tracts46,47 and to infer ancestry independently of reference genomes (that is, allowing detection of admixture from unknown source populations)48. Second, because a number of new sequencing technologies rely on fragmentation during the library preparation stage, degraded DNA from museum specimens and the subfossil record can be incorporated into genomic studies49,50.

Recently, vonHoldt et al.51 used whole-genome data to document widespread ancient hybridization and introgression in North American canids, suggesting that eastern and red wolf (Canis lupus lycaon and Canis lupus rufus, respectively) genomes contain significant contributions from gray wolves (Canis lupus) and coyotes (Canis latrans) to their ancestry and may be of hybrid origin. Similarly, Svardal et al.52 provided evidence of ancient admixture in vervet monkeys (Chlorocebus pygerythrus). Interestingly, many studies reporting ancient hybridization are focused on mammals (see also ref. 53), a significant advance since Stebbins3 pointed out that few studies of hybridization in mammals existed. In other taxa, it has been difficult to distinguish ancient hybridization from other processes like whole-genome duplications until recently. For example, results from whole-genome studies in baker’s yeast (Saccharomyces cerevisiae) have clarified the evolutionary history of this economically important fungus. It appears that hybridization did play a role in the evolution of baker’s yeast and that this hybridization event was followed by a whole-genome duplication34 (see also ref. 54).

Paleogenomic studies are playing a major role in furthering the understanding of the frequency and taxonomic distribution of ancient hybridization. Most recently, ancient admixture has been documented between brown and polar bears (Ursus arctos and Ursus maritimus) and appears to have been widespread during the last glacial maximum, when polar bear distributions were more expansive than those at present day55. These findings have important implications for understanding outcomes of hybridization as polar bear distributions contract and hybridization with brown bears once again becomes common. Ancient hybridization has also been rigorously documented between humans and Neanderthals24,56,57. Finally, complex hybridization dynamics in elephantids (including extinct straight-tusked elephants (Palaeoloxodon antiquus) and mammoths (Mammuthus spp.)) have recently been reported29. It appears that interspecies hybridization was a common occurrence between straight-tusked elephants and extant forest elephants (Loxodonta cyclotis) when their ranges broadly overlapped, and the authors29 present evidence of widespread hybridization between mammoths along a band of range overlap.

Understanding the long-term outcomes of ancient hybridization is difficult. On the timescale of multiple generations, Schumer et al.36 examined replicate hybrid populations of swordtail fishes (Xiphophorus spp.) and found that the maintenance of assortative mating and the genomic distribution of hybrid ancestry varied significantly among hybrid lineages, even though they all arose from the same two hybridizing parents. Overall, we still have much to learn about how genomes evolve following hybridization events33, particularly the role of selection in purging introgressed alleles58,59. This should be a major focus as studies document additional cases of ancient hybridization. In some taxa24, it appears that selection following hybridization resulted in regions of the genome devoid of genetic material from one of the hybridizing taxa. For the human–Neanderthal example, there is potential evidence that genes underlying skin and hair color conferred adaptive advantages following introgression. However, throughout the human genome there is a dearth of Neanderthal ancestry56,57, especially on the sex chromosomes25, which may play significant roles in the maintenance of Neanderthal and human lineages. New methods that are being developed to test for selection against introgression across whole-genome data46,47 will allow an unprecedented look at the long-term consequences of hybridization.

Certain outcomes of ancient hybridization are of particular interest. The role that hybridization may play in adaptive radiations was theorized by Seehausen13, and recent results using genome-spanning data in African cichlids have provided support for the idea that hybrid swarms can provide the genetic novelty for adaptive radiations30,31,60. Seehausen13 hypothesised that a number of other adaptive radiations may have been the product of (or have been facilitated by) rampant hybridization (for example, Darwin’s finches), within which genome-spanning data have documented widespread hybridization61. Given how significantly the resolution of genomic data in many systems has changed since 2004, it will be exciting to see if this hypothesis holds up for other classic adaptive radiations like Lake Baikal sculpin (Abyssocottidae), Hawaiian honeycreepers (Drepanididae), silverswords (Argyroxiphium sandwicense), or Laupaula spp. crickets13. Indeed, a recent review of the genomics of adaptive radiations reported evidence for hybridization in all systems for which multiple sequenced genomes exist62.

Given the number of new systems within which ancient hybridization has been documented, it seems likely that, as additional studies are conducted in a greater number of taxa, evidence of ancient hybridization will increase. An important consideration with respect to ancient hybridization is contemporary conservation. How should detection of ancient hybridization influence conservation63? Current policies have provisions for hybridization, but many are focused at the level of species. The results reported by vonHoldt et al.51 and Toews et al.35 are both interesting cases where hybridization appears to have played a major role in the evolutionary history of taxa currently listed, or that are being considered for listing, under the Endangered Species Act. As the understanding of the frequency of ancient hybridization increases, it should inform policy63.

Challenges of demonstrating adaptive introgression

It is likely that hybridization often leads to the introgression of adaptive gene regions64,65,66; however, it is necessary to demonstrate an adaptive function for the introgressed genomic regions before claiming the discovery of adaptive introgression65. In their recent review of adaptive introgression, Arnold and Kunte64 state that there is overwhelming evidence for the occurrence of adaptive introgression but acknowledge the need for, and frequent absence of, fitness estimates. Importantly, for a number of examples of adaptive introgression that they highlight, no direct link has been made between genotype and phenotype, and no adaptive function of phenotype has been rigorously demonstrated (see Tables S1a and S1b in ref. 64). Demonstrating the adaptive function of a specific gene region is a difficult task in many systems and will remain a challenge. This is especially true for organisms that cannot be easily incorporated into experiments (for example, free living wolves and tropical birds). In the absence of experiments that convincingly demonstrate an adaptive function of a specific genomic region, methods that detect signatures of positive selection can be used65,67; however, inferring adaptive introgression from genomic signatures alone should be done with caution and is best coupled with functional gene annotation68. Further, few tests for positive selection are designed for admixed genomes, and phenomena like heterosis can generate signals of positive selection in the absence of adaptive introgression69. There is thus a critical need for the development of new methods. Although linking introgression of specific genomic regions to phenotypes with demonstrated adaptive functions is rare and difficult, several recent examples that use whole-genome data exist in the literature (Fig. 2 and Table 1).

Table 1 A selection of recent studies in speciation

Not surprisingly, it is easiest to link introgression to adaptive functions when the introgressed region confers drug or disease resistance70,71 or when the gene region is responsible for a well-studied trait (for example, wing color pattern72,73). This most often occurs for phenotypic traits controlled by single genes of large effect or when multiple genes for a given phenotypic trait are on the same chromosome67 or linked in an inversion74,75. Perhaps the biggest advance in our understanding of adaptive introgression is that we can now link specific genomic regions to their phenotypic trait, which was difficult (except in model organisms) until very recently. By taking advantage of natural admixture, researchers can now pinpoint gene regions that underlie phenotypes of interest with known adaptive functions, and they can then examine the behavior of these genomic regions when hybridization occurs76.

A number of recent studies that report adaptive introgression following hybridization have used both whole-genome and experimental data (Fig. 2 and Table 1). Liu et al.71, following up on Song et al.70, confirmed recent adaptive introgression of an allele conferring warfarin resistance from Mus spretus to Mus musculus domesticus and also report two previously unknown ancient hybridization events between these lineages. Suarez-Gonzalez et al.67 reported adaptive introgression from Populus balsamifera to Populus trichocarpa. Importantly, they used whole-chromosome sequencing to investigate specific gene regions for which they also evaluated function in a common garden; they then linked these functions back to patterns of introgression in the wild. Similar inferences have been made for the common bean (Phaseolus vulgaris) by Rendon-Anaya et al.77; however, the adaptive function of introgressed regions was inferred using genomic analyses rather than common gardens. Jones et al.76 used whole-exome and whole-genome sequencing to uncover the genetic basis of seasonal coat color change in snowshoe hares (Lepus americanus) and went on to demonstrate that the allele that confers brown coat color likely introgressed into the snowshoe hare genome from the closely related black-tailed jackrabbit (Lepus californicus) (Fig. 2). In this case, the adaptive function of the introgressed allele is clear: hares that do not match their background experience higher rates of mortality78. These new studies take advantage of whole-genome data paired with fitness estimates and functional understanding of traits to rigorously document adaptive introgression in nature. Adaptive introgression is likely more common than was once assumed; however, we caution against making inferences of adaptive introgression in the absence of appropriate data, such as fitness estimates and a demonstrated adaptive function for a specific gene region. Although these examples focus on a single gene of large effect or taxa for which experimental studies in common gardens are possible, it is exciting that the linking of genotype to phenotype in many different systems is increasingly becoming achievable.

Hybrid speciation is a rare phenomenon

Hybrid speciation is defined as a speciation event in which hybridization has played a crucial role in the evolution of reproductive barriers between a hybrid lineage and its parent lineages. There are two major types of hybrid speciation: allopolyploid and homoploid. Allopolyploid hybrid speciation is defined as the formation of a hybrid lineage concomitant with a whole-genome duplication, which results in immediate incompatibility between the hybrid and their parent species. The combination of parental genomes in allopolyploid hybrids likely favours their establishment in unique niches, and we are learning a great deal about the genetic architecture and mechanistic origins of polyploid genomes using genomic approaches79,80. In homoploid hybrid speciation, the resulting hybrid lineage does not undergo a genome duplication, yet the combination of parental genomes also must lead to traits that isolate hybrids from the parent species16,81. The emphasis on hybridization directly contributing to the evolution of reproductive isolation is important but continues to generate debate in the evolutionary biology community82,83. It is not sufficient to infer hybrid speciation from mosaic ancestry alone. Admixture could represent what remains after hybrid ancestry has been purged from critical regions of the genome58,59. The classic examples of homoploid hybrid speciation are the Helianthus sunflowers. Three independent lineages have evolved from hybridization between H. annuus and H. petiolaris84. Helianthus fulfill the three criteria that define a hybrid species: (1) hybrid lineages are reproductively isolated from their parent lineages through genomic rearrangements and adaptation to xeric or saline habitats uninhabitable to the parent species84, (2) they have been clearly demonstrated to be a product of hybridization, in this case through lab studies that recreated the genomic composition of hybrid lineages85, and (3) hybridization led directly to the extreme phenotypes that allowed hybrids to persist in xeric or saline habitats86.

Among recent claims of hybrid speciation, two examples are supported by evidence of reproductive isolation stemming from hybridization (Fig. 3). Lamichhaney et al.87 use a long-term field study of Darwin’s Finch (Geospiza fortis × Geospiza conirostris) to directly document homoploid hybrid speciation, from initial hybridization to reproductive isolation of the hybrid lineage after only three generations. Although the timescale of their study is short from an evolutionary perspective, they convincingly demonstrate the speed with which reproductive isolation can be reached between hybrids and their parental taxa. It remains unclear, however, how long these barriers will last given the potential for stochastic habitat changes and negative effects of inbreeding. In the budding yeast Saccharomyces paradoxus, a very different organism, Leducq et al.88,89 used whole-genome sequencing and found evidence supporting homoploid hybrid speciation. They suggest that chromosomal architecture in the hybrid lineage plays a role in the maintenance of reproductive isolation between that lineage and the parental taxa and also report that the hybrid lineage inhabits a unique ecological niche that may further isolate it from the parental taxa.

Even in the absence of clear evidence for homoploid hybrid speciation, the role of hybridization and introgression in the evolution of many taxa is interesting in and of itself. Some intriguing examples of potential hybrid speciation that were difficult to study without whole-genome data come from a variety of fungi (see Table 1 in refs. 90,91). A common theme among these studies is the suggestion that having a hybrid origin has allowed these fungi to colonize novel environments and/or hosts or to become more pathogenic than their parental taxa88,89. Further, many of these species have implications for human health92,93 or agriculture94. The morphological similarity of many of these taxa has previously made it impossible to know if hybridization played a role in their evolution. In many of these cases, it is difficult to determine if hybridization per se contributed to reproductive isolation between the hybrid taxon and the parental taxa. That said, Leducq et al.89 provide convincing evidence that the hybrid species is reproductively isolated from its parental taxa owing to chromosomal incompatibilities. Similar investigations should be carried out in other fungal systems to fully evaluate the status of these taxa as homoploid hybrid species.

Additional recent examples of possible hybrid speciation based on genome-wide analyses come from nematodes and birds. Lunt et al.37 use whole-genome data and report complex hybrid origins of a widely distributed crop pest within the root knot nematode group (Meloidogyne spp.). They confirm a previous hypothesis that the widespread tropical species, M. incognita, is of hybrid origin—a double-hybrid derived from one hybrid parent species (M. floridensis) and an unknown parent species. Lunt et al.37 hypothesize that the complex hybrid origin of M. incognita has facilitated the increased pathogenicity of the species, which is considered to be one of the most important tropical crop pests around the globe. The extent of reproductive isolation of the hybrid lineage remains unknown in this case, but is assumed to be significant.

Two other bird species, the Italian sparrow (Passer italiae) and the golden-crowned manakin (Lepidothrix vilasboasi), are proposed to be of hybrid origin and have been examined using high-resolution genomic data sets42,43,95,96,97,98. Elgvin et al.98 document mosaic genomic inheritance and genomic divergence in the Italian sparrow that is novel compared with its purported parental taxa, the house (Passer domesticus) and Spanish (Passer hispaniolensis) sparrows. Runemark et al.42,43 found consistent patterns of variation in specific genomic regions of Italian sparrows from populations on four islands in the Mediterranean, interpreted as constraint on the composition of hybrid genomes. Unlike Lamichhaney et al.87, these studies have inferred reproductive isolation from patterns in genetic and genomic data and, although hybridization has played a role in these population’s evolutionary history, it remains unclear if they fulfill the criteria for homoploid hybrid speciation99. Additional field-based data on reproductive isolation will help fill this knowledge gap.

Clearly, there are an increasing number of taxa for which hybridization has likely played an important role in their evolution. Some appear to have a history of hybridization, but whether they are homoploid hybrid species or have experienced ongoing or irregular gene flow with close relatives throughout their evolutionary history remains unclear in most cases. Generally, however, there is insufficient data to demonstrate homoploid hybrid speciation. Prematurely labelling a lineage a homoploid hybrid species leads to a misunderstanding of the frequency and importance of homoploid hybrid speciation versus the contributions that ancient and contemporary hybridization and adaptive introgression (previously discussed) can make to genomic variation within species16,83. It will be important to incorporate statistical tests that account for the timing of hybridization100 in future studies of hybrid speciation.

Conclusions and looking forward

Admittedly, the three broad discussion points in this Review are less distinct than they have been presented. Ancient introgression may often have been adaptive, but our ability to directly link introgression to adaptation in most systems is limited. Before labelling something as adaptive, which often happens in the absence of sufficient data, it is critically important to demonstrate adaptive function. At the same time, it is important to recognize that even if hybridization leads to introgression of adaptive alleles, it can also lead to strong negative selection against foreign alleles24. Moving forward, haplotype-based investigations of hybridization should be adopted whenever possible to provide greater insight into the breakdown of linkage blocks and the generality of genomic architecture following contemporary and ancient hybridization101. We recognize, however, that this will require better ancestry inference and phasing approaches than currently exist for most species, which is an avenue of future research.

It is an exciting time to study hybridization, and it is a time during which researchers should utilize model-based estimates, incorporate natural selection and geographic variation, explicitly measure reproductive isolation in the field, and work on hybrid zones where backcrossing and introgression occur5,33. Increased genomic resolution is offering insight into the importance and prevalance of hybridization not possible even 10 years ago. As more studies of a diverse array of taxa are accumulated, scientists will be able to generate a robust understanding of the role of ancient hybridization across taxa, link introgression to adaptive functions, and rigorously test the requirements of homoploid hybrid speciation. These advances will continue to illuminate how hybridization has played a creative force in the generation of Earth’s biodiversity.

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Acknowledgements

We thank D. Jackson for assistance with figure design.

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Taylor, S.A., Larson, E.L. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nat Ecol Evol 3, 170–177 (2019). https://doi.org/10.1038/s41559-018-0777-y

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