Version: 16 February 2016
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)
Mallet: Hybrid Speciation
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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?
Mallet: Hybrid Speciation
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"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
Mallet: Hybrid Speciation
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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]
Mallet: Hybrid Speciation
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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
Mallet: Hybrid Speciation
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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
Mallet: Hybrid Speciation
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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
Mallet: Hybrid Speciation
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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 shiftingbalance-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.
Mallet: Hybrid Speciation
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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.
Mallet: Hybrid Speciation
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In plants about 20 well-established homoploid hybrid species are known24, 27,
but they are hard to detect and may be much commoner. The bestdocumented 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
Mallet: Hybrid Speciation
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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 welldocumented genetic intermediacy between parent species, is a homoploid
hybrid form of the butterfly Lycaeides. The hybrid form inhabits highelevation 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
Mallet: Hybrid Speciation
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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?
Mallet: Hybrid Speciation
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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
Mallet: Hybrid Speciation
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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
Mallet: Hybrid Speciation
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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.
Mallet: Hybrid Speciation
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Figure 1. Hybridization and the adaptive landscape
polyploid hybrid
species 1
homoploid hybrid
phenotype
species 2
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.
Mallet: Hybrid Speciation
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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 OA .
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.
Mallet: Hybrid Speciation
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Table 1. A selection of hybrid species
Hybrid
species
Common
name
Senecio
cambrensis
ragwort a
composite
plant
Helianthus
anomala,
H. deserticola,
H. paradoxus
sunflowers
Spartina
anglica
smooth
cord-grass
Parent species Ploidy
(speciation
mechanism)
S. squalidus
hexaploid
(introduced
(allopolyploidy)
diploid),
S. vulgaris
(native
tetraploid)
H. annuus
diploid
(diploid),
(homoploidy)
H. petiolaris
(diploid)
tetraploid
(allopolyploidy)
Rhagoletis
unnamed sp.
S. maritima
(native),
S. alterniflora
(introduced)
freshwater B. tropicus
snail
group species
(carries
schistosomiasis)
stick insect B. rossius,
B. grandii
stick insect B. rossius,
B. grandii,
B. atticus
Lonicera
R. mendax,
fly
R. zephyria
Lycaeides
unnamed sp.
blue
butterfly
L. idas,
L. melissa
Heliconius
heurippa
Bulinus
truncatus
Sexuality
Adaptations of
hybrid species
self-fertile
outcrossing
hermaphrodite
Successful
colonizer in Wales
(extinct in
Scotland)22
largely selfincompatible
outcrossing
hermaphrodites
outcrossing
hermaphrodite
Desert adaptations
inherited as QTLs
from appropriate
parents25
tetraploid
(probable
allopolyploidy)
selfer
diploid
(homoploidy)
triploid
(allopolyploidy)
asexual
diploid
(homoploidy)
dioecious
diploid
(homoploidy)
dioecious
heliconian
butterfly
H. melpomene, diploid
H. cydno
(homoploidy)
dioecious
Gila seminuda
Virgin
River chub
(a fish)
G. robusta,
G. elegans
diploid
(homoploidy)
dioecious
Cottus sp.
invasive
sculpin
C. perifretum,
C. rhenanus
diploid
(homoploidy)
dioecious
Bacillus whitei
Bacillus
lynceorum
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asexual
Survives further
downshore than
parents, global
range spread23
Successful
colonizer outside
range of parents11
Successful
competition11
Successful
competition11
Novel host fruit:
introduced
Lonicera species31
Novel host plant
and novel alpine
habitat30
Colour pattern
inhibits mating
with either
parent32
Inhabits tributary
of Colorado river
from which
parents excluded29
Invasion of
warmer and more
turbid water28
18
1.
Lotsy, J.P. Evolution by Means of Hybridization (Martinus Nijhoff, The Hague,
1916).
2.
Mayr, E. Animal Species and Evolution (Harvard University Press, Cambridge,
Mass., 1963).
3.
Stebbins, G.L. Processes of Organic Evolution (Prentice-Hall, Englewood
Cliffs, New Jersey, 1971).
4.
Grant, V. Plant Speciation (Columbia Univ. Press, New York, 1981).
5.
Barton, N.H. The role of hybridization in evolution. Molec. Ecol. 10, 551-568
(2001).
6.
Coyne, J.A. & Orr, H.A. Speciation (Sinauer Associates, Sunderland, Mass.,
2004).
7.
Anderson, E. & Stebbins, G.L. Hybridization as an evolutionary stimulus.
Evolution 8, 378-388 (1954).
8.
Arnold, M.L. Natural Hybridization and Evolution (Oxford University Press,
Oxford, 1997).
9.
Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198207 (2004).
10. Dowling, T.E. & Secor, C.L. The role of hybridization and introgression in the
diversification of animals. Ann. Rev. Ecol. Syst. 28, 593-620 (1997).
11. Bullini, L. Origin and evolution of animal hybrid species. Trends Ecol. Evol. 9,
422-426 (1994).
12. Grant, P.R., Grant, B.R., & Petren, K. Hybridization in the recent past. Amer.
Nat. 166, 56-57 (2005).
13. Fisher, R.A. The Genetical Theory of Natural Selection (Clarendon Press,
Oxford, 1930).
14. Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20,
229-237 (2005).
15. Otto, S.P. & Whitton, J. Polyploid incidence and evolution. Ann. Rev. Genet. 34,
401-437 (2000).
16. Ramsey, J. & Schemske, D.W. Neopolyploidy in flowering plants. Ann. Rev.
Ecol. Syst. 33, 589-639 (2002).
17. Husband, B.C. Constraints on polyploid evolution: a test of the minority
cytotype exclusion principle. Proc. Roy. Soc. Lond. B 267, 217-223
(2000).
Mallet: Hybrid Speciation
19
18. Astaurov, B.L. Experimental polyploidy in animals. Ann. Rev. Genet. 3, 99-126
(1969).
19. Muller, H.J. Why polyploidy is rarer in animals than in plants. Amer. Nat. 59,
346-353 (1925).
20. Mable, B.K. 'Why polyploidy is rarer in animals than in plants': myths and
mechanisms. Biol. J. Linn. Soc. 82, 453-466 (2004).
21. Brochmann, C. et al. Polyploidy in arctic plants. Biol. J. Linn. Soc. 82, 521-536
(2004).
22. Abbott, R.J. & Lowe, A.J. Origins, establishment and evolution of new
polyploid species: Senecio cambrensis and S. eboracensis in the British
Isles. Biol. J. Linn. Soc. 82, 467-474 (2004).
23. Ainouche, M.L., Baumel, A., & Salmon, A. Spartina anglica C. E. Hubbard: a
natural model system for analysing early evolutionary changes that affect
allopolyploid genomes. Biol. J. Linn. Soc. 82, 475-484 (2004).
24. Rieseberg, L.H. Hybrid origins of plant species. Ann. Rev. Ecol. Syst. 28, 359389 (1997).
25. Rieseberg, L.H., Raymond, O., Rosenthal, D.M., Lai, Z., & Livingstone, K.
Major ecological transitions in wild sunflowers facilitated by
hybridization. Science 301, 1211-1216 (2003).
26. Buerkle, C.A., Morris, R.J., Asmussen, M.A., & Rieseberg, L.H. The likelihood
of homoploid hybrid speciation. Heredity 84, 441-451 (2000).
27. Gross, B.L. & Rieseberg, L.H. The ecological genetics of homoploid hybrid
speciation. J. Hered. 96, 241-252 (2005).
28. Nolte, A.W., Freyhof, J., Stemshorn, K.C., & Tautz, D. An invasive lineage of
sculpins, Cottus sp. (Pisces, Teleostei) in the Rhine with new habitat
adaptations has originated from hybridization between old
phylogeographic groups. Proc. Roy. Soc. B 272, 2379-2387 (2005).
29. DeMarais, B.D., Dowling, T.E., Douglas, M.E., Minckley, W.L., & Marsh, P.C.
Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive
hybridization: implications for evolution and conservation. Proc. Natl.
Acad. Sci. , USA 89, 2747-2751 (1992).
30. Gompert, Z., Fordyce, J.A., Forister, M., Shapiro, A.M., & Nice, C.C.
Homoploid hybrid speciation in an extreme habitat. Science 314, 19231925 (2006).
31. Schwarz, D., Matta, B.M., Shakir-Botteri, N.L., & McPheron, B.A. Host shift to
an invasive plant triggers rapid animal hybrid speciation. Nature 436,
546-549 (2005).
32. Mavárez, J. et al. Speciation by hybridization in Heliconius butterflies. Nature
441, 868-871 (2006).
Mallet: Hybrid Speciation
20
33. Meyer, A., Salzburger, W., & Schartl, M. Hybrid origin of a swordtail species
(Teleostei: Xiphophorus clemenciae) driven by sexual selection. Molec.
Ecol. 15, 721-730 (2006).
34. Labandeira, C.C. & Sepkoski, J.J. Insect diversity in the fossil record. Science
261, 310-315 (1993).
35. Butlin, R. Speciation by reinforcement. Trends Ecol. Evol. 2, 8-12 (1987).
36. Patterson, N., Richter, D.J., Gnerre, S., Lander, E.S., & Reich, D. Genetic
evidence for complex speciation of humans and chimpanzees. Nature
441, 1103-1108 (2006).
37. Evans, P.D., Mekel-Bobrov, N., Vallender, E.J., Hudson, R.R., & Lahn, B.T.
Evidence that the adaptive allele of the brain size gene microcephalin
introgressed into Homo sapiens from an archaic Homo lineage. Proc.
Natl. Acad. Sci. , USA xxx, online: 0606966103 (2006).
38. Barton, N.H. How did the human species form? Current Biology 16, R647-R650
(2006).
39. Wright, S. The roles of mutation, inbreeding, crossbreeding and selection in
evolution. Proc. XI Int. Congr. Genet. Hague 1, 356-366 (1932).
40. Orr, H.A. The population genetics of adaptation: the distribution of factors fixed
during adaptive evolution. Evolution 52, 935-949 (1998).
41. Coyne, J.A., Barton, N.H., & Turelli, M. Is Wright's shifting balance process
important in evolution? Evolution 54, 306-317 (2000).
Mallet: Hybrid Speciation
21