doi: 10.1111/jeb.12038
COMMENTARY
Hybridization may rarely
promote speciation
M. R. SERVEDIO*, J. HERMISSON†
& G. S. VAN DOORN‡
*Department of Biology, University of North Carolina, Chapel Hill, NC, USA
†Mathematics and Biosciences Group, Max F. Perutz Laboratories and Faculty
of Mathematics, University of Vienna, Vienna, Austria
‡Institute of Ecology and Evolution, University of Bern, Hinterkappelen,
Switzerland
Abbott et al. (2013) point out many of the multitude of
ways in which hybridization and speciation interact.
The classical view of the speciation process is that it
occurs most easily in strict allopatry and that it is inhibited by gene flow. Recently, however, the focus of
research has shifted into examining ways in which
hybridization can actually promote the speciation process. Empirical evidence for the facilitation of speciation
by hybridization is often mixed or incomplete, and
some of the mechanisms proposed in the review by
Abbott et al. (2013) are theoretically poorly understood
or controversial. Below, we raise some cautionary notes
on these mechanisms. We conclude that the conditions
under which hybridization can promote speciation may
be more restrictive than the review by Abbott et al.
(2013) implies.
The possibility that hybridization can, counter to initial impressions, actually promote speciation is certainly
intriguing. Homoploid and allopolyploid hybrid speciation, which Abbott et al. (2013) write extensively
about, are two processes by which hybridization can
enable potentially rapid speciation. Abbott et al. (2013)
also, however, discuss several ways in which hybridization may contribute to a more gradual build-up of
reproductive isolating mechanisms; these are more controversial.
The most classic of these is perhaps the process of
reinforcement, whereby the evolution of reproductive
isolation is promoted by selection against interspecific
matings, including by low hybrid fitness (Dobzhansky,
1940; Servedio & Noor, 2003). Reinforcement has long
been recognized as a way in which speciation may
proceed, at least to some degree, when hybridization is
occurring. A process analogous to reinforcement is
‘adaptive speciation’, in which speciation begins in
sympatry and continues as hybridization (in the sense
of continued gene flow) between the incipient species
is occurring. Mathematical models of this process are in
Correspondence: Maria R. Servedio, Department of Biology, University of
North Carolina, Chapel Hill, NC 27599, USA.
Tel.: +1 919 843 2692; fax: +1 919 962 1625;
e-mail: [email protected]
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many ways identical to reinforcement models, albeit
with different starting conditions; they can thus be discussed together. Many theoretical models have found
favourable conditions for reinforcement and adaptive
speciation, and empirical evidence also suggests that
reinforcement, at least, may not be uncommon (see
Coyne & Orr, 2004). One important question that
relates to whether hybridization promotes speciation is
whether reinforcement merely allows speciation to
proceed despite gene flow or whether it actually speeds
up the process of divergence. There is some evidence,
though taxonomically restricted, that suggests the latter
(e.g. Coyne & Orr, 1989, 2004).
However, there are a number of theoretical reasons, increasingly well understood in recent years, to
be cautious about the generality of this finding. The
spread of alleles leading to increased reproductive isolation has been found to be very slow in several
mathematical models of speciation with gene flow
(e.g. Bolnick, 2004; Proulx & Servedio, 2009), and
other models suggest that the degree of trait divergence or reproductive isolation that evolves may be
limited (e.g. Kirkpatrick & Servedio, 1999; Matessi
et al., 2001; Kirkpatrick, 2000; Pennings et al., 2008;
Servedio, 2011; but see Bank et al., 2012a). These
limitations are often due to the fact that the evolution of premating isolation during reinforcement and
adaptive speciation relies on linkage disequilibrium
between the genes that cause reproductive isolation
and the genes under selection (those, for example,
that cause low hybrid fitness); this genetic association is
often weak, whereas gene flow itself is relatively strong
(Kirkpatrick, 2000; note that, in reinforcement models,
weaker gene flow reduces the occurrence of selection
against hybrids as well, so the qualitative relationship
between the forces does not change). Additional obstacles to speciation with gene flow are created by positive
frequency-dependent sexual selection undermining species coexistence, stabilizing sexual selection acting
against the divergence of mating strategies, the loss of
genetic variation in traits underlying assortment and
the effects of search costs (e.g. Matessi et al., 2001; van
Doorn et al., 2004; Kirkpatrick & Nuismer, 2004; Bürger
& Schneider, 2006; Kopp & Hermisson, 2008; Otto
et al., 2008; Pennings et al., 2008). There are several
mitigating factors that may increase the likelihood or
extent of reinforcement and adaptive speciation, including very specific types of selection (e.g. van Doorn
et al., 2009), certain mutational step sizes of assortment
combined with specific geographic conditions (e.g.
Rettelbach et al., 2011; Servedio, 2011; Bank et al.,
2012a) or the presence of ‘magic’ traits that are both
under divergent selection and are targets of assortment
(Gavrilets, 2004). It is not known how often any of
these mitigating conditions will occur.
Abbott et al. (2013) also suggest that hybridization
may contribute to speciation by acting as a source of
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Commentary
adaptive variation. They argue that because mutation is
rare, hybridization may be an important source of
selectively favoured alleles in a population and that this
may be especially true when the species in question are
closely related. Consider, however, that new sister
species, A and B, have recently shared a common gene
pool. If a variant is favoured in one of the sister species,
B, but is not currently present in it, we can presume
that it was likely absent in the standing genetic variation of the ancestral population. In that case, however,
in order for species B to get this variant from species
A, this favourable mutation must arise and spread in A;
in other words, we still have to wait for mutation.
Depending on the relative population sizes, this is not
likely to speed up adaptation significantly over waiting
for the mutation in population B alone. Abbott et al.
(2013) also discuss the case of favoured combinations
of linked loci introgressing from one species into
another. We agree that this may promote adaptation in
a species, but it is perhaps more likely in species that
have diverged less recently.
Nevertheless, if hybridization does increase the
spread of adaptive variants in a species, does this
mean that it promotes speciation? Abbott et al. (2013)
suggest a causal relationship between the two processes in this section of their paper stating that ‘introgression could have important implications for the
origin of species’ and that ‘hybridization might contribute to adaptive divergence between populations’.
Yet adaptation does not equal divergence or the
build-up of reproductive isolation. If an adaptive variant spreads from one population to another, this
makes the two species more alike, not more different.
In other words, the introgression of a variant that is
adaptive in both populations will tend to homogenize
the two.
The only case in which divergence would be promoted is if a variant were present, yet deleterious, in
one species (species A) and were yet at an appreciable enough frequency to introgress into a second species (species B) in which it was beneficial, but
initially absent. The spread of a novel deleterious
mutation to a high frequency in a population (species
A, in this case) is relatively rare, and it is likely that
only a small proportion of such alleles would be beneficial in a sister species (species B). This may be
especially true if the two species are closely related
and share a largely common genetic background. The
scenario outlined in this paragraph seems especially
unlikely for the case of a complex of linked loci,
which would essentially never be able to assemble in
a population (species A) in which the complex phenotype was selected against.
One could imagine situations in which an environmental shift makes a formerly favoured (and thus
prevalent) allele (or complex of alleles) in species A
suddenly deleterious, but a simultaneous initiation of
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contact with a species B in which such an allele is
favoured seems far-fetched. Also, a scenario of colonization or invasion of species A into the range of species
B does not make introgression likely to further separate
the species, because the allele in question would still
presumably be favoured in the population of species A
in its original range, even if it were deleterious in
invading individuals. Finally, even if the spread of a
single divergently selected allele were to occur via
introgression (the case in which a deleterious allele
spreads into a species in which it is beneficial), the
question remains whether the resulting amount of
divergence would outweigh the homogenizing effect of
gene flow at other loci in the genome to promote,
instead of retarding, overall differentiation. In sum, we
believe that the idea that adaptive introgression would
promote speciation is very unlikely to hold up in a
mathematical model of this process.
An interesting way in which hybridization might
promote speciation is presented by Abbott et al. (2013)
as a potential ultimate consequence of reinforcement in
cases in which there is only partial geographic overlap
of populations. Abbott et al. (2013) argue that within
one species, evolution in an area of sympatry with a
congener can lead to the initiation of reproductive isolation between a population in this area and one in an
area in which the initial species is the only one present
(an allopatric area). Under what conditions might this
occur? If there are relatively homogeneous selective
conditions within each species, such isolation may persist only if the gene flow between populations of the
initial species is very low. If this is not the case, reproductive isolation genes can easily spread to the other
populations of the initial species, quickly eroding the
newly formed reproductive barrier. This problem applies
particularly to mating preferences, as these are in most
cases subject to weak selection, implying that they are
effectively homogenized across populations by gene
flow.
Reproductive isolation between the populations of
the initial species in sympatry and allopatry would
thus be unlikely to persist unless these populations
are themselves subject to divergent selection. Abbott
et al. (2013) themselves describe the phenomenon
potentially occurring in ‘patchy environments’, which
implies selective differences. They also cite several
empirical examples of the evolution of reproductive
isolation that match the scenario described above, so
it would seem that sometimes these conditions are
met. Three points to consider are as follows. First,
the evolution of some reproductive isolation between
sympatric and allopatric populations within one of
the species in contact would be promoted if there
were simply selection in the sympatric population
against mating attempts with heterospecifics, even
without hybridization per se (e.g. even if offspring of
mixed ancestry were not produced, following the
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M. R. SERVEDIO ET AL.
definition of hybridization given in Abbott et al.
2013). In fact, any adaptation arising from interspecific interactions in one area but not the other could
potentially lead to divergent selection between the
two (Pfennig & Pfennig, 2010). Thus, hybridization
itself is not facilitating speciation in this scenario,
but merely tends to erode any evolving differences due
to the homogenizing effects of gene flow. Second, the
initiation of some reproductive isolation between two
populations of a species does not mean that this isolation will continue to develop to the point of speciation.
Many of the myriad of reasons that speciation with gene
flow is difficult apply directly to the completion of speciation in this situation. Finally, if selection is already
divergent between two populations of one of the species
in secondary contact, speciation might proceed without
any hybridization or interspecific interactions, although
it is possible that the contact event may facilitate the
initial stages of the process.
Even if gene flow may promote speciation only under
special circumstances, hybridization is certainly not
antithetical to the eventual build-up of reproductive
isolation. The question is not whether speciation despite
gene flow is possible at all, but how it would proceed – and
whether it leaves a clear signature for us to detect. Abbott
et al. (2013) discuss several intriguing ideas connected
with this question, such as the build-up of speciation
islands or of consensus clines. As the authors point out,
these issues still rely largely on vague and verbal arguments and call for further study, both theoretically and
empirically.
An emerging consensus that is worth pointing out
concerns the crucial role of adaptive evolution during
scenarios of speciation with gene flow. This is obvious
for reinforcement and adaptive speciation. But the
build-up of post-zygotic barriers due to accumulating
Dobzhansky–Muller incompatibilities (DMIs) also seems
to require that evolution of the barrier alleles is driven
by positive selection. Empirically, all hybrid incompatibilities that have been detected in Drosophila carry
adaptive signatures (Presgraves, 2010). Theoretically,
Bank et al. (2012b) show that the evolution of DMIs
under any level of gene flow stronger than drift
requires that DMI’s are adaptive. Moreover, selection
must be heterogeneous across subpopulations. In contrast, true local adaptation is not strictly necessary, that
is, each DMI allele individually can be beneficial in
both populations. The latter scenario usually requires a
specific order in the appearance of the DMI alleles during evolutionary history (mutation order speciation,
Schluter, 2009).
To conclude, we fully agree with Abbott et al. (2013)
that the impact of hybridization on speciation is a
highly important field for further study. However, the
main reason for this may not be that hybridization
opens a fast track to speciation, but quite simply that
hybridization and gene flow are pervasive in nature.
Acknowledgments
MRS was supported by NSF Grant DEB 0919018. JH
acknowledges funding from the Vienna Science and
Technology Fund (WWTF) through grant MA06-01.
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Received 17 August 2012; revised 28 September 2012; accepted 5
October 2012
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