Eukaryote hybrid genomes result from interspecific hybridization, where closely related species mate and produce offspring with admixed genomes. The advent of large-scale genomic sequencing 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 may 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 adaptation or speciation makes hybrid genomes a particularly exciting subject in evolutionary biology. The article summarizes 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. This article reviews 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 this article focuses on interspecific hybridization (referred to as hybridization in this review).
Evolutionary outcomes
There are several potential evolutionary outcomes of hybridization. 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). 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 backcrossing 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 is described 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, 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.
Detection and study with genomic tools Many empirical case studies start with exploratory detection of putative hybrid taxa or individuals with genomic clustering approaches, such as those used in the software 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 statistics 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.
Hybrid species definition 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 Moharrek et al. 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.