Hybrid speciation




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Hybrid speciation
James Mallet
("Progress" article for Nature)

Galton Laboratory, Department of Biology, University College London,



4 Stephenson Way, London UK, NW1 2HE
Corresponding author: James Mallet (j.mallet@ucl.ac.uk)

Botanists have long held that hybrid speciation is important in plants, especially via chromosomal doubling or allopolyploidy. Until recently it was argued that hybridization rarely played such a creative role in animals. Today, advances in genetics are showing that hybrid speciation, even without polyploidy, is commoner in plants and also animals than we thought.
Linnaeus famously stated in Systema Naturae that species have remained unchanged since the dawn of time, but his experiments with plants later led him to conclude that hybridization provided a means of species modification. Ninety years ago, Lotsy1 still argued that species were invariant genetic types, and that novel lineages could evolve only via hybridization. These peculiar ideas about species were overturned by the 1950s, when the concept emerged that species are reproductively isolated populations2-4. In zoology, this species concept discouraged ideas that hybridization and gene flow (introgression) between species could be important evolutionary forces2, 5, 6, even while botanists continued to argue for their significance4, 7, 8. Today, armed with new and abundant molecular marker data, biologists are finding that hybridization can be important in speciation and adaptive radiation in animals as well as plants8-12.
What is hybrid speciation?
"Hybrid speciation" implies that hybridization has played a major role in the origin of a species. In the case of hybrid species that have doubled their chromosome number (allopolyploidy), the definition is clear because a new species contains exactly one genome from each parent, a 50% contribution from each. Furthermore, allopolyploids are largely reproductively isolated by ploidy. In recombinational hybrid speciation where the chromosome number has not doubled (homoploid hybrid speciation), the definition is less clear. The fraction of the genome from each parent will rarely be 50%, especially if backcrossing is involved. Homoploid hybrid species may be only weakly reproductively isolated, and are hard to distinguish from species which have gained alleles from other species by hybridization and introgression, or from persistent ancestral polymorphisms. Although hybrid speciation is sometimes inferred if any marker alleles originate from different parents, I here restrict the term to cases where hybrid allelic combinations contribute to the spread of novel, stabilized hybrid lineages.
[Fig. 1 somewhere here]
Theory and background of hybrid speciation
Hybridization may be "the grossest blunder in sexual preference which we can conceive of an animal making"13, but it is nonetheless a regular event in many organisms. The fraction of species that hybridize is variable, but on average around 10% of animal and 25% of plant species are known to hybridize with at least one other species14. Hybridization is much more extensive in some rapidly radiating groups; 75% of British ducks (Anatidae)14, for example. Recent, closely related species are most likely to hybridize, often for millions of years after initial divergence14. At the population level, however, hybridization is of course unusual. Less than 0.1% of individuals in a typical population are interspecific hybrids2, 14. Hybridization is thus a normal feature of species, if at a rather extreme end of the natural spectrum of sexual genetic exchange5. Hybrid offspring, on the other hand, are "hopeful monsters" with hefty differences from both parents, and little apparent scope for survival (Fig. 1, Box 1). Furthermore, hybrids are often sterile or inviable due to divergent evolution in each species2, 6.
Yet hybrid species exist. What advantages could outweigh the seemingly insurmountable problems to allow the formation of new species? This innocent-sounding question plunges to the heart of controversies about adaptive evolution. Is saltational evolution possible, and are maladaptive intermediates and genetic drift involved? Common sense and prevailing opinion suggests that evolution normally occurs by small adjustments rather than saltation, and rarely involves maladaption6. Hybrid speciation may violate both rules (Box 1). Two major types of hybrid speciation are treated here: speciation via allopolyploidy and homoploid hybrid speciation.
[Box 1 somewhere here]
Hybrid speciation via allopolyploidy

Polyploidy is a well-established mode of speciation in plants, though many aspects of polyploid evolution are only today being uncovered3, 15, 16. Speciation can be via autopolyploidy (duplication of chromosomes within a species) or allopolyploidy (duplication of chromosomes in hybrids between species), though the boundary between the two is somewhat blurred because of the fuzzy nature of species. All polyploid species are reproductively isolated from their parents because when polyploids mate with diploids, progeny with odd-numbered ploidys are produced. These offspring may be viable but usually produce sterile gametes with unbalanced chromosomal complements (aneuploidy). Polyploidy is thus a simple saltational means of achieving speciation4. The process may be repeated many times, leading to lineages with >80-fold ploidy in some vascular plants; 40-70% of all plant species are polyploids15.


Allopolyploid speciation can occur via somatic chromosome doubling in a diploid hybrid, followed by selfing to produce a tetraploid. This was the route taken by Primula kewensis, the famous allopolyploid that arose spontaneously in 1909 among cultivated diploid hybrids of P. verticillata and P. floribunda16. However, there are other possibilities, such as fusion of two unreduced gametes after failure of reduction divisions in meiosis. Another likely route is the "triploid bridge," in which a rare unreduced (diploid) gamete fuses with a normal haploid gamete to form a triploid. Triploids are normally sterile, but can contribute to tetraploid formation by themselves producing occasional unreduced triploid gametes, which backcross with a normal haploid gamete to form tetraploid progeny16, 17. This was the route used to create the first, and maybe the only synthetic, self-sustaining bisexual animal allopolyploid strain, in hybrids between the silk moths Bombyx mori and B. mandarina18.
After polyploid hybrids arise, they face major hurdles to establishment. Diploid and triploid hybrids are strongly disfavoured because their aneuploid gametes are almost completely sterile. When even-numbered allopolyploidy is achieved, chromosome pairing is still rarely perfect16. Furthermore, new polyploids tend to be rare and mate mostly with incompatible parentals, giving a minority cytotype disadvantage17. These problems almost certainly explain why bisexual polyploid speciation is much more common in plants than animals: (1) plants more often grow indeterminately, so that somatic chromosome doubling can lead to germ-line polyploidy; (2) plants are also often perennial, or clonally reproducing, allowing multigenerational persistence of hybrid tissues in which polyploid mutations can occur; and (3) they are more often hermaphrodites, allowing selfing as a means of sexual reproduction of rare polyploids, once formed. As expected, polyploidy is strongly associated with asexual reproduction, selfing and perenniality in plants, as well as in animals11, 15, 18. In animals, reversion to outcrossing by polyploids is rare, whereas in plants, with frequent alternation between clonal and sexual phases, bisexual polyploid species are common and themselves often give rise to further species. Thus animal allopolyploids like stick insects (Bacillus) and freshwater snails (Bulinus truncatus) are often, though not always15, parthenogenetic or selfers (Table 1). Muller's theory19 that sex chromosomes in animals prevent sexual polyploidy due to sex:autosome gene dosage is no longer given much credence6, 15, 18, 20.
How common is polyploid speciation? Otto & Whitton15 estimated this from the overrepresentation of even-numbered chromosome counts. Around 2-4% of speciation events in flowering plants and 7% of speciation events in ferns can be explained by recent polyploidy, and this is probably an underestimate6 (40-70% of plant species overall are polyploid, but this includes effects of much non-polyploid speciation within already polyploid lineages15). In animals, there is no bias towards even-numbered chromosomal counts, suggesting that animal polyploid speciation is very rare compared to other speciation modes15.
It used to be thought that allopolyploidy arose more readily than autopolyploidy because new autopolyploids had more chromosome pairing problems in meiosis4. Today, newly arisen autopolyploids are known to have comparable levels of infertility and aneuploid gametes16. More importantly, what is the fraction of allopolyploids among polyploids that spread successfully? There are few studies of large floras, although a small-scale survey in the USA revealed that 79-96% of 28 polyploid species were allopolyploids4. Recently, the Arctic flora was surveyed, where about 50% of the often clonal or selfing species are polyploids21. In Svalbard (Spitsbergen) 78% of the 161 species are polyploid, with average ploidy approximately hexaploid. Every one of 47 polyploid species studied genetically has fixed marker heterozygosity, implying 100% allopolyploidy21. If Svalbard is typical, most successful polyploids are also hybrid species.
After formation, novel hybrid species face the usual "hopeful monster" difficulties (Fig. 1). It helps if they can exploit a new ecological niche which is both vacant and also somewhat spatially separated to ameliorate minority cytotype disadvantage. For example, recent allopolyploid hybrids between introduced and native plants have successfully spread from sites of origin (e.g. Senecio cambrensis in Wales22 and Spartina anglica in England23, Table 1). These invasive allopolyploids were able to exploit vacant ecological roles with relatively little evolutionary change after hybridization (Fig. 1).
Stochastic drift may also be necessary to overcome minority cytotype and other disadvantages. A few polyploids, usually from the same hybridization event, must accumulate locally for the process to take off, implying a shifting-balance-like process (Box 1). Stochastic effects are evident in nature. An independently derived Scottish population of S. cambrensis has gone extinct in Edinburgh some 20 years after its first record22. Allopolyploid hybrids can arise repeatedly from the same parents, but many widespread polyploids (e.g. Spartina anglica, Table 1) probably originated only once or a few times15, 22, 23, even though parent species are in broad contact, again showing the importance of stochasticity and drift in the origins of hybrid species.

Recombinational and homoploid hybrid speciation
Homoploid hybrid speciation or recombinational speciation is well-known in flowering plants, although inferred to be rare4, 7. Speciation takes place in sympatry (by definition, since hybridization requires gene flow), while hybrids must also overcome unfitness, due to chromosomal and genic incompatibilities, in the absence of reproductive isolation via polyploidy. For these reasons, the process is seen as unlikely and infrequent5, 6, 24.
However, hybridization can boost genetic variance25, 26 allowing colonization of unexploited niches (Fig. 1). Suppose + and  alleles at genes affecting quantitative trait differ between species, so that each has fixed differences (+++, and ++, say). Recombination can then liberate "transgressive" quantitative variation25, often more extreme than either parent (e.g.  and +++++). Most early recombinants will be unfit, but extreme hybrids may colonize niches unavailable to parents. If ecological opportunities are partially separated from the parental habitat, if like hybrids tend to associate (for example, via phenology or drift in small populations), or if selfing or inbreeding is common, gene flow between hybrids and parents will be reduced and hybrid speciation becomes more likely7, 25. Hybrid lineages may also displace one or both of their parents26, thereby obliterating evidence of hybrid origin.
In plants about 20 well-established homoploid hybrid species are known24, 27, but they are hard to detect and may be much commoner. The best-documented are the desert sunflowers Helianthus anomalus, H. deserticola and H. paradoxus (Table 1), which all derive from hybrids between mesic-adapted H. annuus and H. petiolaris26, 27. Selfing is rare and provides little assistance to establishment, but the three hybrid species survive drought better than either parent, suggesting recruitment of hybrid transgressive variation. Synthetic hybrid populations are readily recreated with karyotypic combinations similar to wild hybrid species, because selection favours the same combinations of compatible chromosomal rearrangements. In addition, the contribution of adaptive traits for extreme morphology, physiology and life history of the hybrids (for example small leaf size, seed dormancy, or tolerance of drought and salt) from each parent agrees largely with predictions25, 27. In Helianthus, recombinant genotypes and spatial separation of desert habitat from the parent species have enabled the hybrids to survive where their parents are absent.
Although bisexual polyploids are often barred in animals, there is no reason why homoploid hybrid species would be rarer in animals than in plants. Many suspected cases are known10, 27. A recent example is the invasive sculpin, a hybrid fish derived from the Cottus gobio group from the Scheldt River (c.f. C. perifretum) and upper tributaries of the Rhine (c.f. C. rhenanum) (Table 1). Sculpins are normally restricted to clear, well-oxygenated cold waters in upper river tributaries across Europe. The Rhine and Scheldt rivers became connected as a result of earlier canal building, but invasive sculpins appeared in the warmer and muddier lower Rhine only in the last 15 years. Morphologically, the invasive sculpin is intermediate, and has mitochondrial, SNP and microsatellite variants characteristic of both Scheldt and Rhine forms28. The hybrid form meets Rhine sculpins in narrow hybrid zones, but remains distinct despite gene flow, suggesting that it is adapted mainly to the lower Rhine. The recent evolution and spread of the invasive sculpin, as well as its intermediacy, provides convincing evidence of recent, adaptive hybrid origin. A more ancient example is the cyprinid fish Gila seminuda, which inhabits the Virgin River, a tributary of the Colorado River (USA) (Table 1). The putative hybrid species contacts but does not overlap its parent species, G. robusta and G. elegans from the Colorado River. Gila seminuda is morphologically and genetically intermediate, and morphologically similar to synthetic hybrids. The intermediacy of the hybrid form may allow it to outcompete both parents in the Virgin River29. A similar case, with well-documented genetic intermediacy between parent species, is a homoploid hybrid form of the butterfly Lycaeides. The hybrid form inhabits high-elevation alpine habitats not occupied by either parent, as well as using a different host plant30.
Rhagoletis fruitflies provide a further historically documented example. In 1997 flies were first found on introduced honeysuckle (Lonicera spp.) (Table 1). Molecular markers in the fly are characteristic of both parents, the blueberry maggot R. mendax and the snowberry maggot R. zephyria31. No F1 genotypes have been detected between the hybrid form and its parents where they overlap; the new fly is reproductively isolated. Rhagoletis flies mate on host fruits, and host choice therefore ensures mating specificity. The Colombian butterfly Heliconius heurippa32 suggests a different route to hybrid speciation. This form has a colour pattern like that of synthetic hybrids between local H. cydno and H. melpomene. Microsatellite alleles are shared between all three species, but H. heurippa forms an allele frequency cluster distinguishable from both H. cydno and H. melpomene. Intermediate wing colours of H. heurippa are used as a cue in mating discrimination, and directly cause reproductive isolation from either parent. Similarly, in the fish Xiphophorus clemenciae, the "sword tail", a hybridization-derived trait, is involved in sexual selection and mate choice33.
Hybrid speciation in animals is so far supported by few molecular data. Genomic mapping of ecological or speciation-related hybrid QTLs, which so strongly supports hybrid speciation in Helianthus, is not yet available for any animal case. Many homoploid hybrid species fail to overlap with at least one parent species, and reproductive isolation is weak, so species status could be questioned (the Lonicera-feeding Rhagoletis is an exception). Nonetheless, in all these cases hybrid traits seem to contribute to maintenance or ecological expansion of the new taxa.
Is hybrid speciation important in evolution?
There are now plenty of examples of hybrid speciation. We know that polyploidy is common in plants, giving rise to 2-7% of vascular plant species, but rarer in animals. Furthermore, ancient polyploidy seems common at the root of many plant and animal groups. Genome duplications very likely contributed to the evolution of complex organisms (though this is debated)15, and we can infer that most successful genome duplications were allopolyploid, if evidence from plants is correct4, 21. Hybridization would then be at the root not just of speciation events, but also of major evolutionary innovations.
Polyploid speciation leaves a clear genomic signature, but we have little idea how common homoploid hybrid speciation is. We know that hybridization and introgression between species is a regular occurrence, especially in rapidly radiating groups9, 12, 14. Most speciation involves natural selection6, natural selection requires genetic variation, and genetic variation is enhanced by hybridization12. Enough suspected homoploid hybrid species exist to indicate that it may be as common in animals as in plants, in contrast to the situation for polyploidy, and no obvious reproductive syndrome prevents its occurrence in animals. Nonetheless there are still not many confirmed cases, but this could mainly be because of the difficulty of demonstrating that hybridization has led to speciation. In particular, we need better genomic analyses of putative hybrid species. As for the hybrid species as a whole, we have observed synthetic or recent speciation in seven genera discussed here (Helianthus, Senecio, Primula, Spartina, Rhagoletis, Bombyx, and Cottus), and there are many other cases. It would be hard to find another mode of speciation so readily documented historically and so amenable to experimentation.
That hybrid species exist at all reveals something unexpected about adaptive landscapes (Fig. 1). If hybrid "hopeful monsters" with all their problems ever survive and compete with their parents, they must be able to hit (and for polyploid species, hit almost exactly) new adaptive combinations. This implies both that many adaptive peaks are scattered about in the adaptive landscape, and also that there is much niche-space available for new species. A liberal adaptive landscape is also supported by the success of many introduced non-hybrid species, and resonates with some fossil evidence: for insects, angiosperms, and many other groups, diversity seems to have been increasing more or less continuously over geological time34.
Mating barriers seem unlikely to evolve via selection against the production of unfit hybrids ("reinforcement"), because recombination would almost always dissociate genes for mating preference from those affecting hybrid inviability and sterility35. We now know of many ecological races or species that remain distinct in the face of significant gene flow and introgression6, 8, 14. In these taxa, reinforcement will not face the problem of too much recombination because distinctness is already maintained. Reinforcement may thus be more common than previously suspected6. In reinforcement, genes important to speciation evolve within each species rather than via introgression. Although this is not hybrid speciation, hybridization nonetheless clearly contributes to speciation.
The ability of hybrid species to invade hitherto unoccupied niches (Table 1) will also mean that hybridization can contribute strongly to adaptive radiations such as African cichlids and Darwin's finches7, 9, 12. This is also well demonstrated by the "domestication niche". Humans have unwittingly created many allopolyploid and other hybrid crops and domestic animals while selecting for transgressively high yields4, 7. Even our own species may have a hybrid genetic ancestry36, 37, though this is contested38. Whichever way this debate is resolved, it would hardly be surprising if hybridization had triggered the origin of Homo sapiens, the most invasive mammal on the planet37.

Acknowledgments

I thank Christian Brochmann, Kanchon Dasmahapatra, Brian Husband, Sandra Knapp, Mauricio Linares, Jesús Mavárez, Axel Meyer, Patrik Nosil, Camilo Salazar, "Spot" Turelli and three anonymous referees for discussions and comments. The work was supported in part by grants from NERC and the DEFRA Darwin Initiative programme.



Figure 1. Hybridization and the adaptive landscape

The hyperspace of possible phenotypes and genotypes can be represented as an adaptive landscape39. Fitness optima ("adaptive peaks") are shaded. Adaptive landscapes are not rigid, but are readily distorted by environmental or biotic changes, including evolutionary change. Mean phenotypes of species and their hybrids are shown as crosses, and offspring distributions as dots. Species 1 and 2 are adapted to different fitness optima. Natural selection acts mainly within each species, so hybrids are "hopeful monsters" far from phenotypic optima. It is therefore hard to imagine how hybrids often attain new optima unless unoccupied adaptive peaks are abundant.


Polyploid hybrids have a variety of advantages, including heterozygote advantage, extreme phenotypic traits and reproductive isolation. Genetic variation in their offspring is not much greater than that of their non-hybrid parents because recombination between parental genomes is rare4, 16, so hybrids cannot spread unless already near an optimum. Homoploid hybrids have fewer initial advantages, but their progeny can have extremely high genetic variances via recombination, including phenotypes more extreme than either parent – transgressive variation (not shown here). This burst of variation can help homoploids attain new adaptive peaks far from parental optima.

Box 1. Competing theories of adaptive evolution
A. Fisher/Orr theory of adaptation
Fisher13 argued that natural selection would mostly fix mutations with very small adaptive effects. Imagine an adaptive goal or optimum, O, in multidimensional phenotype space. If a population's phenotype is currently at point A, the population can be imagined to be on the surface of a hypersphere with centre O, and radius . Only mutations landing within the sphere are favoured. A mutation with very small effect has a ~50% chance of falling inside the sphere, because the surface of the sphere is effectively flat relative to the small mutation size. The larger the mutational effect, the lower the probability of improvement, an effect which is more severe as more phenotypic dimensions are added. Fisher's argument appears to prove that adaptations must be constructed by many tiny individual mutations.

Fisher's argument was incomplete. It ignored two important factors. First, Fisher himself had demonstrated that the fate of most weakly advantageous mutations was to be lost by random drift13. Even if a mutation has a considerable selective advantage, say 1%, the probability of eventual spread is only ~1/50. The larger the advantage, the less likely it is lost. Second, Orr40 showed that large mutations would often be fixed during adaptation. Large effect mutations are rarely beneficial, but, when they are, they contribute to rapid shifts in the mean, and so a few big, advantageous mutations tend to be fixed before many smaller mutations finish the process. Under a variety of assumptions, the distribution of mutational effects fixed is expected to be approximately exponential5, 40. This revised Fisher/Orr theory shows how hybridization with a large effect can contribute to adaptation, even though it produces large shifts in the adaptive landscape (Fig. 1).


B. Wright's shifting balance theory of adaptation
According to Wright39, Fisher's theory of adaptation was incomplete for a different reason. In Fisher's theory, populations can climb local optima, but crossing maladaptive valleys towards new, even more adaptive peaks is impossible (Fig. 1). Wright argued that valleys may sometimes be crossed by means of stochastic genetic drift, perhaps aided by reduced or fluctuating selection, or, as here, hybridization. If multiple loosely connected populations in a species experiment in this way, some may approach a new peak – Phase I of the shifting balance. Phase II consists of Fisherian climbing of the new adaptive peak. Finally, in Phase III, greater productivity of populations at new, more adaptive optima enhances export of adaptations to other populations. Wright argued that his was a more complete theory because inter-population processes of genetic drift and gene flow are considered together with mutation and selection within populations. It added group selection to the theory of adaptation39. Today, the shifting balance is an unpopular theory of adaptation because requirements for stochasticity in small local populations are stringent, and because of doubts about Phase III41. However, hybrid speciation provides an excellent potential example. Hybrid populations will often be maladapted, as well as suffering minority disadvantages. If a small hybrid population with an adaptive phenotype overcomes its minority disadvantage via drift (often aided by selfing), it can spread at the expense of its parents, and, most importantly, colonize new ecological opportunities.

Table 1. A selection of hybrid species




Hybrid species

Common name

Parent species

Ploidy (speciation mechanism)

Sexuality

Adaptations of hybrid species

Senecio cambrensis

ragwort a composite plant

S. squalidus (introduced diploid),

S. vulgaris (native tetraploid)

hexaploid

(allopolyploidy)



self-fertile outcrossing herm-aphrodite

Successful colonizer in Wales (extinct in Scotland)22

Helianthus anomala,

H. deserticola,

H. paradoxus

sunflowers

H. annuus (diploid),

H. petiolaris

(diploid)



diploid

(homoploidy)



largely self-incompatible outcrossing herm-aphrodites

Desert adaptations inherited as QTLs from appropriate parents25

Spartina anglica

smooth cord-grass

S. maritima (native),

S. alterniflora (introduced)

tetraploid

(allopolyploidy)



outcrossing herm-aphrodite

Survives further downshore than parents, global range spread23

Bulinus truncatus

freshwater snail

B. tropicus group species (carries schisto-somiasis)

tetraploid

(probable allopolyploidy)



selfer

Successful colonizer outside range of parents11

Bacillus whitei

stick insect

B. rossius,

B. grandii

diploid

(homoploidy)



asexual

Successful competition11

Bacillus lynceorum

stick insect

B. rossius,

B. grandii,

B. atticus

triploid

(allopolyploidy)



asexual

Successful competition11

Rhagoletis unnamed sp.

Lonicera fly

R. mendax,

R. zephyria

diploid

(homoploidy)



dioecious

Novel host fruit: introduced Lonicera species31

Lycaeides unnamed sp.

blue butterfly

L. idas,

L. melissa

diploid

(homoploidy)



dioecious

Novel host plant and novel alpine habitat30

Heliconius heurippa

heliconian butterfly

H. melpomene,

H. cydno

diploid

(homoploidy)



dioecious

Colour pattern inhibits mating with either parent32

Gila seminuda

Virgin River chub (a fish)

G. robusta,

G. elegans

diploid

(homoploidy)



dioecious

Inhabits tributary of Colorado river from which parents excluded29

Cottus sp.

invasive sculpin

C. perifretum,

C. rhenanus

diploid

(homoploidy)



dioecious

Invasion of warmer and more turbid water28

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Mallet: Hybrid Speciation


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