Trends in Ecology & Evolution
Hybridization as an invasion of the genome
Introduction
Formless pods drift through space. They land on Earth. The pods germinate, and the developing embryos take on features of the individual humans that they will eventually replace. A chilling scenario emerges: an invasion has occurred and humanity is being taken over by an alien species with an agenda very different to our own. The 1956 cult movie ‘Invasion of the Body Snatchers’ achieves suspense by playing on our fear of infiltration and genetic usurpation.
Also around this time, the so-called ‘biological’ species concept, having been promoted widely for about a decade 1, 2, became the prevailing view of species among evolutionary biologists. This viewpoint argued that species, unlike races or genera, were ‘real’ and had special, species-level qualities: ‘isolating mechanisms’, ‘cohesion’, and ‘coadapted gene complexes’; species acted as vessels for the ‘storage and protection of genetic variation.’ Even today, many branches of biology continue to see species as discrete and fundamental units, rather than as poorly differentiated way-stations in a continuous hierarchy of biodiversity.
Hybridization (see Glossary) and introgression between species is the converse of reproductive isolation and challenges the ‘reality’ of biological species. In the course of the development of the biological species concept, a sort of repugnance against hybridization prevailed, akin to the fear on which ‘Invasion of the Body Snatchers’ plays. Supporters of the biological species concept viewed hybridization as a ‘breakdown of isolating mechanisms’ [2]. When hybridization occurred, it was explained via species range changes and environmental disturbance, mostly as a result of human habitat alteration. F1 hybrids are generally less viable and fertile (even given some hybrid vigour). Backcrossed genotypes, if produced, are often inferior, so that introgression was assumed to be rare; if it did occur it was thought to lead only to deleterious effects [2]. These almost eugenic views about species were particularly prevalent among zoologists because of Ernst Mayr's influence. (By contrast, many botanists thought that introgression was common and important in adaptive evolution.) The same views led directly to the notorious hybrid policy of the US Endangered Species Act of 1973, by which ‘hybrids’ were deemed unworthy of conservation, whereas unsullied ‘pure species’ were apportioned higher status [3]. But today, tastes in biodiversity are changing, and the biological species concept is under attack: in 1990, the hybrid policy was rescinded [4].
Hybridization has been known at least since the time of Linnaeus, and has been discussed frequently by evolutionists 2, 5, 6 following Darwin's lead in the chapter ‘Hybridism,’ where he demonstrated the lack of a clear boundary between varieties and species [7]. Here, I collate and review lesser-known comparative data on natural hybridization rates and discuss results from newer, molecular methods for the detection of hybridization and introgression, rather than covering the subject in toto. Much of the best literature on natural hybridization is about plants, but I concentrate particularly on animal data because zoologists have traditionally been more skeptical about the importance of introgression.
I also attempt lay to rest our almost instinctive, common-sense view that hybridization is always unnatural or extremely rare (see also [5]). In zoology, we tend automatically to assume that hybridization is a ‘reproductive mistake’. For example, from an excellent discussion on hybridization in birds of paradise, we read: ‘We presume that a male will mate with whatever bird solicits his copulation – another weakness in the system that might allow hybridization’ ([8], my emphasis). It is indeed probable that mating systems have often evolved to prevent this ‘weakness’, but we can no longer take it for granted that hybridization is a ‘weakness’ a priori. For example, natural hybrids among Darwin's finches are fitter than purebreds, at least under current climatic conditions on Galapagos, very probably because the avoidance of deleterious homozygosity by outcrossing outweighs whatever benefits there might be of choosing mates from within the species [9]. Selection will regulate deleterious hybridization, but the selection pressure on the parents against hybridization can never be greater than the fraction of the population hybridizing; as soon as hybridization becomes rare, selection might not be strong enough to deliver complete assortative mating. Greatly improved genetic data show clearly that horizontal gene transfer, hybridization, and introgression between species are ongoing and regular, if not always common processes in nature [5]. These discoveries have important implications in conservation [4] as well as in studies of the safety of transgenic crops that might hybridize with wild relatives [10]. Genomic invasions have been occurring at all levels of the Tree of Life since the dawn of evolution, and have contributed considerably to the adaptive radiation and diversification of early life (11, 12 and see below).
Section snippets
The frequency of natural hybridization
Hybridization between species is always rare on a per-individual basis, but this statement is tautological because we would not be able to distinguish species if hybridization were common. Under biological 2, 6 or recognition [13] species concepts, in which species are internally compatible and externally reproductively isolated, hybridization between individuals of separate species is rare by definition. Under phylogenetic or genealogical species concepts, species are defined by fixed, and/or
Is hybridization natural, or are humans to blame?
The frequent examples of hybridization in nature (e.g. Table 1) are often attributed to environmental degradation 2, 6: if hybridization is assumed to be unnatural, its presence must indicate some failure of the ‘balance of nature’. Anderson [23], for example, argued that much hybridization and introgression was a result of ‘hybridization of the habitat’ of separately adapted species, mainly caused by human disturbance. (It is undoubtedly true that some examples of hybridization today, such as
‘Isolating mechanisms’
The low frequency of hybrids between most species, on a per individual basis, is largely explained by prezygotic and postzygotic effects known as ‘isolating mechanisms.’ This term is associated with the biological species concept, and seems to imply that the ‘mechanisms’ have been designed by natural selection to prevent hybridization. Today, a more neutral term such as ‘reproductive barriers’ seems better because much reproductive isolation is ‘unintended’ by natural selection and is instead a
Genetic evidence for hybridization and introgression
Hybridization and introgression are well known in plants. For example, genetic studies confirming hybridization and introgression exist in many taxa long known to produce hybrids, such as Eucalyptus, oaks, and willows 32, 33, 34, and good surveys are available of genetic studies on plants [5]. Hybridization in animals is more controversial, and, as a zoologist, I therefore concentrate on animal data.
Introgression, adaptation, speciation, and biodiversity
As already mentioned, hybridization between introduced and native species can cause problems in conservation 4, 65 and has become an important topic in the debate about the release of transgenic crops [10]. In Europe, hybridization between native white-headed and American ruddy ducks Oxyura is a high-profile example, and introductions of trout for fisheries have been a particular problem for native trout species [4]. Invasion of the genome can be a problem.
But when framing conservation policy,
Acknowledgements
The article was greatly improved thanks to useful suggestions and criticisms from Michael Hochberg, Mohamed Noor, Sally Otto, Clive Stace, Ziheng Yang, and an anonymous reviewer.
Glossary
- Allopatric:
- two groups of populations or species are allopatric if their ranges are not connected; there is a geographic barrier between them that prevents gene flow. Allopatric speciation is therefore speciation in which the whole process takes place under conditions of geographic isolation.
- Assortative mating:
- the tendency for ‘like to mate with like’. Species or morphs within a species are said to mate assortatively if mating is biased towards other individuals with a similar phenotype or
References (92)
The problems with hybrids: setting conservation guidelines
Trends Ecol. Evol.
(2001)A species definition for the Modern Synthesis
Trends Ecol. Evol.
(1995)Does parental divergence predict reproductive compatibility?
Trends Ecol. Evol.
(2002)Asymmetrical introgression in a freshwater fish hybrid zone as revealed by a morphological index of hybridization
Biol. J. Linn. Soc.
(1999)Population biology and conservation of the Corsican swallowtail butterfly Papilio hospiton Géné
Biol. Conserv.
(1996)Systematics and Origin of Species
(1942)Animal Species and Evolution
(1963)- et al.
Bureaucratic mischief: recognizing endangered species and subspecies
Science
(1991) Natural Hybridization and Evolution
(1997)- et al.
Speciation
(2004)
On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life
The Birds of Paradise
Inbreeding and interbreeding in Darwin's finches
Evolution
Genes invading new populations: a risk assessment perspective
Trends Ecol. Evol
Phylogenetic classification and the universal tree
Science
The ring of life provides evidence for a genome fusion origin of eukaryotes
Nature
The recognition concept of species
A local flora and the biological species concept
Am. J. Bot.
The evolution of F1 postzygotic incompatibilities in birds
Evolution
Patterns of speciation in Drosophila revisited
Evolution
Mimicry and warning color at the boundary between races and species
Mimicry: developmental genes that contribute to speciation
Evol. Dev.
Ice sheets promote speciation in boreal birds
Proc. R. Soc. London B Biol. Sci.
The role of reinforcement in speciation: theory and data
Annu. Rev. Ecol. Syst.
Hybridization of the habitat
Evolution
Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations
Evolution
Host-induced assortative mating in host races of the larch budmoth
Evolution
Sympatric speciation in phytophagous insects: moving beyond controversy?
Annu. Rev. Entomol.
Host races in plant-feeding insects and their importance in sympatric speciation
Philos. Trans. R. Soc. London Ser. B
Genetics and morphological evolution in plants
Am. Nat.
Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution
Proc. Natl. Acad. Sci. U. S. A.
Haldane's rule and X-chromosome size in Drosophila
Genetics
Patterns of natural and manipulated hybridization in the genus Eucalyptus L'Herit. – a review
Austral. J. Bot.
Are chloroplast and mitochondrial DNA variation species-independent in oaks?
Evolution
Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone
Mol. Ecol.
A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: support for the reinforcement hypothesis
Evolution
Gene flow between Drosophila pseudoobscura and D. persimilis
Evolution
Drosophila hybrids in nature: proof of gene exchange between sympatric species
Science
Natural interspecific hybridisation of Simulium sanctipauli s.l. with Simulium squamosum and Simulium yahense (Diptera: Simuliidae)
Tropenmed. Parasitol.
Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex
Genetics
Flow of mitochondrial DNA across a species boundary
Proc. Natl. Acad. Sci. U. S. A.
One-way introgression of a subspecific sex-chromosome marker in a hybrid zone
Heredity
Plumage and mtDNA haplotype variation across a moving hybrid zone
Evolution
Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers
Mol. Ecol.
Natural hybrids of Papilio (Insecta: Lepidoptera): poor taxonomy or interesting evolutionary problem?
Can. J. Zool.
Cited by (1623)
Introgressions lead to reference bias in wheat RNA-seq analysis
2024, BMC BiologyWhat determines mate choices? Heterospecific mating in Sympetrum dragonflies
2024, Freshwater Biology