Hybridization as an invasion of the genome

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Hybridization between species is commonplace in plants, but is often seen as unnatural and unusual in animals. Here, I survey studies of natural interspecific hybridization in plants and a variety of animals. At least 25% of plant species and 10% of animal species, mostly the youngest species, are involved in hybridization and potential introgression with other species. Species in nature are often incompletely isolated for millions of years after their formation. Therefore, much evolution of eventual reproductive isolation can occur while nascent species are in gene-flow contact, in sympatry or parapatry, long after divergence begins. Although the relative importance of geographic isolation and gene flow in the origin of species is still unknown, many key processes involved in speciation, such as ‘reinforcement’ of post-mating isolation by the evolution of assortative mating, will have ample opportunity to occur in the presence of continuing gene flow. Today, DNA sequence data and other molecular methods are beginning to show that limited invasions of the genome are widespread, with potentially important consequences in evolutionary biology, speciation, biodiversity, and conservation.

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

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