Download A framework for comparing processes of speciation in the

Molecular Ecology (2011)
doi: 10.1111/j.1365-294X.2011.05350.x
INVITED REVIEW
A framework for comparing processes of speciation
in the presence of gene flow
C A R O L E M . S M A D J A * and R O G E R K . B U T L I N †
*Centre National de la Recherche Scientifique (CNRS), Institut des Sciences de l’Evolution UMR 5554, cc065 Université
Montpellier 2, 34095 Montpellier, France, †Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10
2TN, UK
Abstract
How common is speciation-with-gene-flow? How much does gene flow impact on
speciation? To answer questions like these requires understanding of the common
obstacles to evolving reproductive isolation in the face of gene flow and the factors that
favour this crucial step. We provide a common framework for the ways in which
gene flow opposes speciation and the potential conditions that may ease divergence. This
framework is centred on the challenge shared by most scenarios of speciation-withgene-flow, i.e. the need for coupling among different components of reproductive
isolation. Using this structure, we review and compare the factors favouring speciation
with the intention of providing a more integrated picture of speciation-with-gene-flow.
Keywords: associations, assortative mating, gene flow, phenotypic plasticity, recombinations,
selection, speciation
Received 22 July 2011; revision received 27 September 2011; accepted 2 October 2011
Understanding how speciation occurs in the absence of
geographic barriers has been a source of interest and
debate for the past 50 years. It is now accepted that the
evolution of reproductive barriers without spatial separation or in secondary contact zones is a plausible route
to speciation (Servedio & Noor 2003; Bolnick & Fitzpatrick 2007). More recently, however, the debate has
shifted away from geographic modes and towards the
difficult challenge of assessing the frequency in nature
of speciation processes that involve gene flow and of
elucidating the factors that facilitate their occurrence.
As an illustration of this change, the phrase ‘divergence-with-gene-flow’ or ‘speciation-with-gene-flow’
(Rice & Hostert 1993) has been spreading in the literature, reflecting interest in a more continuous vision of
speciation in time and space (Butlin et al. 2008; Fitzpatrick et al. 2008, 2009; Nosil et al. 2009b; Pinho & Hey
2010). Following this change in focus, research on the
underlying mechanisms has intensified in the past few
Correspondence: Carole Smadja, Fax: +33(0)467143622;
E-mail: [email protected]
2011 Blackwell Publishing Ltd
years, leading to major theoretical and empirical
advances.
Several reviews have echoed the prolific experimental
and theoretical developments in this field of research:
they shed light on particular scenarios favouring divergence in the face of gene flow such as reinforcement
(Servedio & Noor 2003; Ortiz-Barrientos et al. 2009;
Servedio 2009) or sympatric speciation (Bolnick & Fitzpatrick 2007; Fitzpatrick et al. 2008, 2009), the role of
selection (Kirkpatrick & Ravigné 2002; Dieckmann et al.
2004; Gavrilets 2004; Maan & Seehausen 2011) or more
specifically ecologically driven selection (ecological speciation Rundle & Nosil 2005; Hendry 2009; Rundell &
Price 2009; Matsubayashi et al. 2010), or the role of
genetic architecture in speciation (Rieseberg 2001;
Jiggins et al. 2005; Hoffmann & Rieseberg 2008; Nosil
et al. 2009b). Using the insights provided by these previous reviews and considering more recent advances,
we take a broader look at the mechanisms favouring
speciation-with-gene-flow to extract the essential features common to all scenarios and to avoid limiting
our view to specific modalities; and we provide a com-
2 C . M . S M A D J A and R . K . B U T L I N
mon framework in which to discuss and compare the
different factors influencing divergence. We hope that,
by treating speciation-with-gene-flow as a whole, the
general conditions facilitating divergence in the face of
gene flow can be highlighted and a more integrated
picture can be drawn.
Speciation-with-gene-flow: an overview
Speciation-with-gene-flow: mode or mechanism?
What is ‘speciation-with-gene-flow’? Figure 1 provides
a visual representation of various concepts and modes
of speciation as commonly defined in the literature and
in relation to each other. Speciation-with-gene-flow
(orange frame) encompasses multiple previously
defined modes of speciation and treating it as a whole
emphasises the poorly resolved relationships among
other categorisations. It broadly overlaps with cases of
adaptive speciation (purple frame), as most scenarios
involve a dose of disruptive ⁄ divergent selection (Gavrilets 2004), but does not exclude nonadaptive mecha-
nisms (Rundell & Price 2009); second, it includes cases
of ecological speciation (green frame) and more generally of speciation by natural and sexual selection (blue
and yellow frames) occurring with gene flow, and all
cases of speciation by reinforcement (red frame); and
finally, it ranges from de novo divergence in sympatry
to the further evolution of isolating barriers after secondary contact, but excludes cases of instantaneous speciation in sympatry, where no gene flow opposes
divergence (grey frame). This picture provides additional arguments against categorising speciation (Butlin
et al. 2008), as it underlines the fact that many categories and concepts are overlapping and have fuzzy
edges, and that ‘speciation-with-gene-flow’ reflects less
a mode of speciation than the combination of factors
that promote the evolution of reproductive isolation in
the face of homogenising gene flow. By addressing
‘speciation-with-gene-flow’ as a whole, the focus can
be placed on the mechanisms underlying the gradual
evolution of reproductive barriers among entities that
are interconnected, at least at some point in time and
space.
Fig. 1 Speciation-with-gene-flow in context. The figure distinguishes scenarios of speciation with no contact at all between diverging
populations (left of dashed line) from those with geographical or ecological contact at least at some point in time and space (right of
dashed line). The different types of evolutionary and selective forces potentially involved in each scenario (grey text) are used to
define and delimit different modes and mechanisms of speciation (coloured frames).
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FRAMEWORK FOR COMPARING PROCESSES OF SPECIATION 3
Assessing gene flow in time and space
To determine how common cases of speciation in the
presence of gene flow are in nature and how much
gene flow impacts on the outcome of a speciation process, one needs first to demonstrate the presence of
gene flow at some point in time and space during the
speciation process. The fact that differentiated taxa currently share part or all of their distribution ranges, currently exchange genes or experience regimes of
disruptive selection does not confirm that divergence
occurred with gene flow or that divergence will proceed
to completion of reproductive isolation. Shared variation pre-dating speciation may be mistaken for a signature of gene flow between diverging species (Noor &
Bennett 2009), and assessing the timing of gene flow
remains a big challenge. The development of statistical
approaches for inferring gene flow in the history of past
speciation events has significantly advanced this field
(Nielsen & Wakeley 2001; Becquet & Przeworski 2007;
Hey & Nielsen 2007; Hey 2010; Yang 2010). Several
empirical studies have applied these coalescent-based
analyses (e.g. Isolation-Migration, Hey 2006 for a
review) or approximate Bayesian approaches (Cornuet
et al. 2008) to estimate the posterior probability distributions of gene flow parameters, given patterns in
nucleic acid sequences, and have inferred that speciation occurred with gene flow (Kronforst et al. 2006;
Niemiller et al. 2008; Salazar et al. 2008; Stadler et al.
2008; Nadachowska & Babik 2009; Pinho & Hey 2010).
Although the application of such approaches warrants
caution (Niemiller et al. 2010) and the analyses may not
necessarily be robust to violations of some assumptions
of the model (Becquet & Przeworski 2009; Strasburg &
Rieseberg 2010; Gaggiotti 2011), these tools will help to
identify new cases of speciation-with-gene-flow and to
understand how reproductive isolation evolves concurrent to gene flow at the initiation, strengthening and
completion stages of the speciation process (Berner
et al. 2009; Nosil et al. 2009b). However, demonstrating
the presence of gene flow is not enough to gain insights
into the role of gene flow as a major factor influencing
the evolution of reproductive isolation, and an even
greater challenge will be to quantify the amount of gene
flow at different stages of the process.
Effect of gene flow on speciation
The likelihood and the spatial scale of speciation are
influenced by the timing and the strength of gene flow
(Kirkpatrick & Ravigné 2002; Servedio & Noor 2003;
Kisel & Barraclough 2010). Gene flow can increase the
probability of speciation as it can: increase the genetic
variation on which selection can act (Mallet 2005; Nolte
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& Tautz 2010); allow genetic variants from different
populations to come together in a single population, up
to and including the generation of reproductively isolated hybrid taxa (Mavarez et al. 2006; Jiggins et al.
2008); and increase the potential for reinforcement
(Servedio & Kirkpatrick 1997). Theoretical and empirical
studies have argued that an intermediate level of gene
flow is optimal for adaptive divergence (Garant et al.
2007). However, gene flow operates fundamentally in
opposition to speciation through two distinct effects:
diluting divergence at individual loci and creating
opportunities for the break-up of associations among
loci through the effects of recombination and segregation (Felsenstein 1981)(we will hereafter refer to ‘recombination’ as a shortcut for ‘recombination and
segregation’). Therefore, the challenge lies in understanding the factors favouring the evolution of reproductive isolation, despite these two effects of gene flow.
Gavrilets and colleagues have shown how mathematical
models can provide great insights into the potential factors at play in any given system under study (Gavrilets
& Vose 2007; Gavrilets et al. 2007; Duenez-Guzman
et al. 2009; Sadedin et al. 2009; Thibert-Plante & Hendry
2009). Here, we propose a complementary approach.
Without ignoring the differences among various spatial
and temporal contexts, we treat as a whole both the
impediments that gene flow introduces into the speciation process and the potential conditions that may
(a)
(b)
Fig. 2 Coupling of the different components of reproductive
isolation. (a) Components of reproductive isolation: squares
represent isolating traits (IT), and small circles inside each
square represent the number of genes underlying each trait.
Reproductive isolation usually relies on the evolution of several traits involved in different types of isolating barrier. (b)
The trait association (TA) chain represents the series of TAs
(red lines) required for the coupling between the different components of reproductive isolation.
4 C . M . S M A D J A and R . K . B U T L I N
favour divergence, and we define a general framework
within which the likelihood of divergence-with-geneflow can be discussed.
A comparative framework
Evolution of trait associations during speciation:
a proxy for the likelihood of speciation-with-gene-flow
Reproductive isolation is usually multi-genic and has
multiple components (i.e. there are several traits contributing to different reproductive barriers) (Coyne &
Orr 2004; (Fig. 2a). Speciation depends on the availability of suitable genetic variation in the traits underlying
reproductive isolation (Barrett & Schluter 2008), and it
may involve divergence in these traits between subpopulations and commonly progresses towards complete
cessation of gene exchange only when associations are
generated and maintained among these traits without
direct divergent selection acting simultaneously on all
isolating traits (Fig. 2b).
Where associations among different traits that
contribute to reproductive isolation must evolve?
This is the greatest obstacle to the build-up of
reproductive isolation towards completion of speciation
(Felsenstein 1981), particularly where associations must
be generated between directly selected traits and those
involved in prezygotic isolation (Barton & De Cara
2009; Servedio 2009). This focuses attention on the ways
in which isolating traits can become coupled together to
build up a strong barrier to gene exchange and on the
evolutionary forces opposing this coupling.
Traits can be associated as a result of pleiotropy
(Box 1), and associations of this type are particularly
Box 1 Pleiotropy, traits and effects
Pleiotropy is the situation where ‘one allele affects two or more traits’ (Barton et al. 2007). This precise
definition is important for discussions of the role of pleiotropy in speciation. Pleiotropy is a property
of an allele, not of a gene. It is possible for one allelic substitution in a gene to influence two traits,
while others influence only one of the traits, or neither. Thus, referring to ‘pleiotropic genes’ (e.g.
Servedio et al. 2011) is potentially misleading. Similarly, the fact that a particular allele has pleiotropic
effects on two traits does not necessarily mean that other alleles at the same or at other loci will also
have pleiotropic effects. The term ‘pleiotropic trait’ (e.g. Jiggins et al. 2005) should, therefore, be
avoided.
A clear terminology is available from quantitative genetics to deal with multiple-gene, multiple-phenotype relationships. Correlations between traits at the phenotypic level may be partly because of
underlying genetic correlations, and these correlations in turn are partly because of pleiotropy and
partly to linkage disequilibrium (Falconer & Mackay 1996).
There are some pairs of traits that necessarily share a significant part of their underlying genetic or
physiological architecture. An example might be male and female body size, or perhaps a male acoustic signal and female preference that share a common underlying oscillator (Butlin & Ritchie 1989). For
such traits, pleiotropy will be common. Nevertheless, it is perfectly possible for them to be influenced
independently by genetic or environmental changes. We refer to these cases as showing ‘extensive
pleiotropy’ (Fig. 3). They are clearly part of a continuum, but TAs between pairs with strong mechanistic links will evolve more easily than pairs with fewer underlying connections. As a result, they will
facilitate speciation.
We also emphasise the distinction between traits and their effects. Take male tail length as an example. This trait may influence both survival and reproductive success in different environments and
mating success with females that have preferences for long or short tails. The single trait has effects on
fitness and on nonrandom mating. Through both routes it may contribute to reproductive isolation.
Although there are multiple effects, there is only a single trait. We feel that it is not helpful to conflate
this situation with pleiotropy, although others have done so (e.g. ‘pleiotropic effects’ in Jiggins et al.
2005). Keeping to a precise definition of pleiotropy, separating discussion of traits from discussion of
the genetic and environmental effects that generate trait variation, and distinguishing between traits
and their effects, helps to clarify the nature of the TA chain underlying speciation (see main text and
Box 2).
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FRAMEWORK FOR COMPARING PROCESSES OF SPECIATION 5
Box 2 Potential examples of multiple-effect traits
Numerous examples of possible multiple-effect traits have been proposed in recent years, but few
cases have been fully analysed. Work that has focused largely on the signalling component of the
mate recognition system has proposed the existence of multiple effects, typically on local adaptation and signal function, for several types of trait: aposematic traits (e.g. poison frogs Dendrobates
pumilio, Oophaga pumilio, Noonan & Comeault 2009; Reynolds & Fitzpatrick 2007), mimicry traits in
coral reef fish (Puebla et al. 2007) or traits involved in adaptation to foraging in different ecological
niches (e.g. beak size in Darwin’s finches, de León et al. 2010); body size in sticklebacks (McKinnon & Rundle 2002); electric signals in African weakly electric fish (Feulner et al. 2009), see also
Servedio et al. 2011 for more putative examples. However, in most of these examples, the contributions that these traits make to reproductive isolation through their multiple effects have not been
measured and may be limited, partly because preferences must diverge and become associated
with the signals before they contribute to isolation (i.e. they fall into scenario B1a in Fig. 3) and
partly because effect sizes may be small (Haller et al. in press). One of the rare convincing examples where the nature of the link has been defined can be found in Heliconius butterflies. Wing
patterns are thought to have diverged because of strong mimetic selection and also to have a signal function, but mate preference divergence has followed as a result of close physical linkage with
wing pattern loci (Kronforst et al. 2006; Chamberlain et al. 2009). The requirement for this association means that the multiple effects of the wing pattern reduce the length of the TA chain, but do
not remove the need for at least one link to be formed.
In contrast, multiple-effect traits that influence mate preferences have been less studied. There are
some suggestive data in three-spine sticklebacks, in which female visual perception has diverged
between two ecotypes as a result of maximising foraging ability in more or less turbid habitats, this
change being followed by divergence in the male trait to enhance conspicuousness to the perceptual
systems of locally occurring females (Boughman 2001). However, here again, the causal relationship
between vision and preference remains to be tested, and the requirement for association with a signal
trait means that the TA chain has a length of at least one. Other sensory drive cases might also be
relevant in this context (e.g. Lake Victoria cichlid fish, Seehausen et al. 2008).
Heliconius cydno (white) and H. pachinus (yellow). Image Credit:
Marcus R. Kronforst, Harvard University.
2011 Blackwell Publishing Ltd
The pea aphid, Acyrthosiphon pisum. Image Credit: Shipher Wu
(photograph) and Gee-way Lin (aphid provision), National Taiwan University, from http://dx.doi.org/10.1371/image.pbio.
v08.i02.g001.
6 C . M . S M A D J A and R . K . B U T L I N
Probably, the best examples of multiple-effect traits with strong contributions to reproductive isolation concern situations where mating location is correlated with habitat choice (‘habitat mechanism’
Gavrilets 2004) and habitat choice directly evolves under selection (B2 in Fig. 3, TA chain = 0). In this
respect, one of the most compelling cases may be host plant preference in the pea aphid, which
induces assortative mating as a result of mating on the preferred host plants. However, it remains
unclear whether host preference has a direct effect on fitness or has evolved through association with
host performance traits as a result of pleiotropy or very close physical linkage with performance loci
(Hawthorne & Via 2001) (Fig. 3: A2). Additional examples of multiple-effect traits of type B2 (Fig. 3)
could potentially be found in situations where nonrandom mating is mediated by other single traits,
such as immigrant inviability and sterility traits (Nosil et al. 2005), floral trait divergence producing a
pollinator shift (e.g. monkey flowers, Bradshaw & Schemske 2003) or flowering time divergence evolving in association with local adaptation (with a potential example in Howea palms, Savolainen et al.
2006).
Finally, one-allele multiple-effect mechanisms (Fig. 3: B3), potentially the most favourable speciation
scenario of all, suffer from a lack of empirical support. Potential forms of one-allele mechanism, such
as the spread of alleles causing individuals to sexually imprint on parental phenotypes, alleles causing
a reduction in migration rate or alleles leading to self-pollination (Servedio & Noor 2003), may be
promising places to investigate.
favourable for speciation, because recombination cannot
oppose them (Maynard Smith 1966; Gavrilets 2004).
Evolving linkage disequilibrium (LD) among loci
underlying different reproductive isolating traits is the
other way the trait associations (TAs) can form. Given
complete spatial separation, mutation, drift and ⁄ or
selection can promote divergence among populations in
multiple traits, which automatically builds up LD
among loci underlying different reproductive barriers,
and thus generates TAs as a simple consequence of the
isolation. In contrast, when gene flow occurs among
diverging populations, it allows recombination to
oppose the build-up of LD and breakdown pre-existing
LD (Felsenstein 1981), thus preventing the formation of
strong associations between isolating traits or disrupting associations previously formed in allopatry. This is
why forming the connection between the different components of reproductive isolation represents the principal challenge in many scenarios of speciation-withgene-flow, and thus why we advocate a framework
based initially on TAs, followed by consideration of the
factors that ease the generation of associations: anything
that allows an escape from the requirement to build LD
among genes underlying isolating traits or that counteracts the deleterious effect of recombination on LD will
favour speciation.
We note that genome-wide LD is a signature of speciation, reflecting the presence of barriers to gene
exchange. Here, we are not primarily concerned with
this effect of isolation, but rather with the LD that
underlies associations between isolating traits, and so
contributes directly to the evolution of stronger barriers
to gene exchange, for example by bringing together the
effects of local adaptation and assortative mating. In
general, if a trait is under divergent selection, associations between loci influencing the trait will be a direct
consequence of selection (Barton 1983). This can be
extended to responses of multiple traits to selection in
complex environments. Such ‘multifarious’ selection
may provide a stronger barrier to gene flow than selection on a single trait (Nosil et al. 2009a), but completion
of speciation is, nevertheless, likely to depend on the
evolution of assortative mating. Our focus here is on
associations between traits under direct selection and
other traits that potentially contribute to reproductive
isolation, but are not under direct selection, such as
assortative mating traits. Formation of these associations
is the difficult step emphasised by Felsenstein (1981)
and many others (reviewed in Gavrilets 2004) and
which we extend here to include multiple TAs.
General recipe for evolving reproductive isolation
in the face of gene flow
We have identified two ingredients, which, combined
together, summarise the conditions favouring the
evolution of reproductive isolation, despite gene flow:
progress towards speciation is more likely when (i)
fewer traits and TAs are required for the build-up
of reproductive isolation and when (ii) any factor
facilitates the strengthening of individual TAs in the
face of gene flow, and thus favours their evolution and
maintenance.
The first ingredient relates to the complexity of the
TA pattern required for reproductive isolation to
evolve. Completion of speciation may involve forma 2011 Blackwell Publishing Ltd
FRAMEWORK FOR COMPARING PROCESSES OF SPECIATION 7
Type of prezygotic isolating mechanism
The TA chain
Minimum Minimum
number
levels of
of TA
LD
Divergence
required?
Opposed by
gene flow via..
2
2
Yes
Dilution/
recombination
1b- Extensive pleiotropy between signal &
preference
2
1
Yes
Dilution/
recombination
2- Single trait
1
1
Yes
Dilution/
recombination
1
0
Yes
Dilution
A- Indirect selection on non-random mating traits
Post-zygotic isolation Prezygotic isolation
components
components
1a- Signal-preference
signal
preference
(e.g.flowering time, habitat preference, assortment trait)
3- One-allele
(e.g. no migration or assortment allele)
B- Direct selection on non-random mating traits
Post- and pre-zygotic isolation
components
1a- Signal-preference
selection on mating trait
signal
preference
1
1
Yes
Dilution/
recombination
selection on mate preference
signal
preference
1
1
Yes
Dilution/
recombination
1b- Extensive pleiotropy between signal &
preference
1
0
Yes
Dilution
2- Single trait
0
0
Yes
Dilution
3- One-allele
0
0
No
No
Legend: Isolating trait:
Genetic basis:
Direct selection:
Indirect selection:
Fig. 3 Length of the trait association (TA) chain and scenarios of speciation-with-gene-flow. This figure represents the TA chain
under different scenarios of speciation and illustrates the effect of the type of prezygotic mechanisms (1 signal-preference, 2
single-trait, 3 one-allele) and modes of selection (A indirect, B direct) on the likelihood of speciation-with-gene-flow. These factors,
by affecting the number of TAs and the levels of linkage disequilibrium (LD) required, as well as the necessity for divergence at
some traits, influence the effect of gene flow on the evolution of reproductive isolation, and thus strongly impact on the likelihood of
speciation-with-gene-flow.
tion of associations between several traits, starting
with traits under direct selection and extending to
others, which enhance reproductive isolation. We call
this set of correlated traits the ‘TA chain’. The fewer
the links in the chain of associations (i.e. the shorter
TA chain) required to couple the different components of reproductive isolation, the fewer the opportunities that gene flow will have to oppose divergence
or to breakdown the coupling between components of
reproductive isolation, and therefore the easier speciation will be. Therefore, factors reducing the length of
the TA chain will favour speciation-with-gene-flow.
The second ingredient relates to the strength of the
links in the TA chain in the face of gene flow. The
tighter the individual associations become, the more
resistant the chain will be to gene flow, and therefore
any factor that promotes the evolution of an association between a trait pair will tend to favour speciation.
Some aspects of these two ingredients are referred to
in the literature. The ‘levels of LD’ introduced by
Servedio (2009) refers to the necessity of connecting,
2011 Blackwell Publishing Ltd
through linkage disequilibrium, the different components of reproductive isolation; the coupling coefficient
developed by Barton (1983), ratio between effective
selection and recombination, determines the strength
of the general barrier produced by multiple loci; some
review articles addressed the role of reduced recombination (e.g. Kirkpatrick & Barton 2006). In the next
sections, we use the combination of these two ingredients as a framework for reviewing the factors favouring speciation-with-gene-flow.
Factors influencing the length of the trait
association chain
Traits contributing to isolation
Reproductive isolation can result from the accumulation
of postzygotic barriers, prezygotic barriers or a mix of
both (Barton & de Cara 2009), spatial coupling can
favour the build up of these associations (Bierne et al.
2011) and the number of traits and trait associations
8 C . M . S M A D J A and R . K . B U T L I N
required for the build-up of reproductive isolation can
vary but theoretical models have shown that the build
up of reproductive isolation in the face of gene flow commonly requires a trait under divergent selection to
become associated with a source of prezygotic isolation,
which is the ultimate step for most speciation-with-geneflow scenarios (Kirkpatrick & Ravigné 2002; Gavrilets
2004; Servedio 2009). How the type of prezygotic isolating barrier affects the likelihood of speciation can be
determined by its impact on the length of the TA chain
required for nonrandom mating to evolve (Fig. 3).
Reproductive isolation may depend on only a single
trait, in which case no TA is required and speciation is
not opposed by recombination (Fig. 3: B2, B3). If this
trait must diverge between subpopulations to generate
isolation, then gene flow still opposes speciation (Fig. 3:
B2), but this is not necessarily the case (Fig. 3: B3).
Reproductive isolation may require two traits. Here, we
recognise two categories: a postzygotic isolating trait
and a nonrandom mating trait (Fig. 3: A2, A3) or a signal trait and a preference trait (Fig. 3: B1). Selection acts
directly on one trait in each case, and divergence in
this trait is opposed by the diluting effect of gene
flow. Indirect selection acts on the other trait, and so
one TA is required. This may require LD, and so be
opposed by recombination (Fig. 3: A2, B1a), but LD
may not be necessary if the traits are coupled by
extensive pleiotropy (Fig. 3: B1b; Box 1) or if divergence between subpopulations is not required for the
generation of assortative mating (Fig. 3: A3). Finally,
three (or more) traits may be involved in reproductive
isolation (A1) with two (or more) TAs that require LD.
Here, both dilution and recombination oppose speciation most strongly. In what follows, we will discuss
these various scenarios in more detail and relate them
to existing terminology.
The idea that speciation-with-gene-flow is facilitated
by a single trait that is under divergent selection and
also causes assortative mating between diverging subpopulations (Fig. 3: B2) has a long history (Maynard
Smith 1966: ‘pleiotropy model’, Gavrilets 2004: ‘similarity-based’ non-random mating). Flowering time is, perhaps, the most convincing example, as natural selection
can favour divergence in peak flowering time between
habitats, and the resulting divergence clearly reduces
gene flow (Devaux & Lande 2008). Habitat choice, especially host choice in phytophagous insects (Box 2), may
also be a single trait of this type, and the huge diversity
of phytophagous insects is consistent with this being a
path to speciation that has few obstacles.
Felsenstein (1981) introduced the idea of ‘one-allele’
mechanisms for increasing assortative mating; for example, decreased dispersal will be favoured by selection
where there is local adaptation to alternative, spatially
separated habitats. Two traits are involved (dispersal
tendency and an adaptive trait), but dispersal is not
under direct selection. No global association is required
between them, because reduced dispersal is favoured in
both habitats (Balkau & Feldman 1973; Felsenstein
1981), but low dispersal is associated with a different
part of the selected trait distribution in each habitat,
simply because the selected trait differs between habitats (Fig. 3: A3). This is equivalent to the assortative
mating model of Servedio (2000), where divergent selection favours a size difference between two habitats, and
there is a second trait that determines the tendency of
females to prefer to mate with males of similar size.
Size-assortative mating in sticklebacks (Gasterosteus
aculeatus) is a possible example (Vines & Schluter 2006).
Here, strong preference needs to be associated with
large size in one habitat and with small size in the other
habitat so the TA chain has length 1. However, this TA
also arises simply because of the difference in the
selected trait between habitats, it does not require any
linkage disequilibrium, and so it is not opposed by
recombination. Where gene flow is asymmetrical, the
necessary TA may be opposed by both gene flow and
recombination, because the nonrandom mating trait may
only be beneficial in one environment (Servedio 2000).
It is also possible to envisage a one-trait, one-allele
model (Fig. 3: B3), which is characterised by direct
selection favouring the same allele in two subpopulations, whose effect is to increase assortative mating
between subpopulations. One possible example is the
case of imprinting on host features in brood parasitic
birds: increased fidelity of imprinting may be favoured
by natural selection for efficient host usage, but it will
also strengthen assortative mating between populations
utilising different hosts (see other examples in Box 3).
Here, neither gene flow nor recombination opposes progress towards speciation.
An assortative mating trait like flowering time may
not be under direct selection, but progress towards speciation may occur when it becomes associated with an
adaptive trait, or with populations that produce unfit
hybrids (Devaux & Lande 2009; Park Grass Experiment:
Silvertown et al. 2005; Howea palms: Savolainen et al.
2006; Gavrilets et al. 2007; Mimulus: Lowry et al. 2008)
(Fig. 3: A2). This is the type of ‘two-allele’ scenario at
the centre of Felsenstein’s argument that speciation is
opposed by recombination. Indirect selection on the
mating trait is also the scenario generally considered in
models of reinforcement, although direct selection can
also occur in reinforcement scenarios (Servedio 2001;
Servedio & Noor 2003). However, our classification emphasises how reinforcement can involve different
lengths of TA chain. Speciation is likely to be most constrained where assortative mating results from the oper 2011 Blackwell Publishing Ltd
FRAMEWORK FOR COMPARING PROCESSES OF SPECIATION 9
ation of preferences in one sex for signal traits in the
opposite sex. The TA chain can then have length 2 or
more (Fig. 3: A1a) unless the signal and preference are
in some way constrained to evolve together (Fig. 3:
A1b, ‘genetic coupling’ Butlin & Ritchie 1989). In these
scenarios generally (Fig. 3: A1, A2, A3), the direct selection may be divergent or disruptive ecological selection
(resulting in extrinsic postzygotic isolation and ⁄ or components of prezygotic isolation such as immigrant inviability, Nosil et al. 2005), or it may be the result of
intrinsic incompatibilities, especially following secondary contact. Models where TA chains of length 1 and 2
are compared directly, such as Dieckmann & Doebeli
(1999), consistently show that speciation is less likely
with the longer chain. Nevertheless, there are examples
where reproductive isolation has evolved, despite the
need for associations between selected traits, signal and
preference (such as the frog, Litoria genimaculata; Hoskin
et al. 2005).
Selection can act directly on signal or preference traits
(Fig. 3: B1a), and this reduces the length of the TA
chain and the number of traits for which divergence is
required. Sensory drive models of speciation fall into
this category (Boughman 2002; Seehausen et al. 2008). It
is helpful to distinguish these scenarios from cases
where selection acts on a different trait from the signal
or preference, but extensive pleiotropy between the
mating traits automatically produces association
between them (Fig. 3: A1b, Box 1); for example, wing
pattern in Heliconius butterflies is under direct divergent
selection and is also used as a mating signal. The same
trait is involved in both defence against predation and
mate choice, so that any mutation influencing the trait
will alter both fitness and mating signal, although a
separate preference trait must be associated with wing
pattern to generate reproductive isolation. This case fits
scenario B1a (Fig. 3). Pheromones released by the androconia on butterfly wings may also influence mate
choice. Here, the trait under direct selection, colour pattern, is distinct from the signal trait. This case fits scenario A1a (Fig. 3), even though some mutations may
have pleiotropic effects on both colour pattern (and so
fitness) and pheromone production, contributing to the
strength of the association between adaptive and mating traits along with LD between loci that influence
only colour or pheromones.
Overall, this comparison highlights the possible variation in the number of distinct traits contributing to
reproductive barriers and the ways in which they might
be associated. It shows how the force of direct selection
may operate, undiluted, to cause isolation in some
cases, while in others, it must be passed along a chain
of connections, each of which is likely to weaken its
effect. We expect short TA chains to favour speciation
2011 Blackwell Publishing Ltd
relative to long TA chains. Moreover, the requirement
for LD can vary within a particular chain length. Any
aspect of the biology of a species, which tends to make
the total length of the TA chain short and ⁄ or reduce the
requirement for LD, is expected to make speciationwith-gene-flow more likely.
We note that history can be an additional determinant of progress towards speciation, particularly when
there is indirect selection: while establishing a TA chain
of a given length may be difficult if divergence occurs
in situ in sympatry, it can start to evolve as a byproduct of geographic separation, either in allopatry or
in a continuous distribution (Barton & Hewitt 1989).
This can favour the subsequent evolution of nonrandom
mating, once populations are in contact. Accentuation
of plumage differences between collared and pied
flycatchers (Ficedula) in sympatry (Saetre & Saether
2010) may be a case in point.
Multiple-effect traits
The term ‘magic trait’ has recently been widely used to
refer to a trait that contributes to prezygotic isolation,
but evolves under direct selection. The significance of
such traits lies in their simultaneous contribution to two
or more components of reproductive isolation, which
favours speciation in the face of gene flow. The term
was introduced by Gavrilets (2004), but the idea dates
back to Maynard Smith’s (1966) ‘pleiotropy’ model and
Schluter’s (2001) ‘by-product mechanism’ (Schluter
2001). Often used for locally adaptive traits that also
function as mating signals (Gavrilets 2004; Servedio
2009), the same principle applies to any trait that influences more than one component of reproductive isolation (mating signals, mate preference, habitat choice,
intrinsic or extrinsic postzygotic isolation and so on).
From our framework (Fig. 3), it is clear that the main
impact of these traits lies in shortening the TA chain.
We note that although direct selection on the trait
makes the scenario even more favourable, other combinations of effects without direct selection also have the
potential to ease the evolution of reproductive isolation
[e.g. response to host cues generating both habitat and
mate choice in Heliconius butterflies, Melolontha cockchafers and probably other insects (Ruther et al. 2000; Estrada & Gilbert 2010) or mating signals contributing
both to assortative mating and to behavioural sterility
in Chorthippus grasshoppers (Bridle et al. 2006)]. The
range of possible TA chains, with different requirements for LD, is too great to be encompassed by a simple magic vs. nonmagic distinction. Moreover, the use of
the term ‘magic trait’ can misleadingly imply that speciation itself becomes automatic or inevitable where such
traits are involved, which is not true in most cases (see
10 C . M . S M A D J A and R . K . B U T L I N
Fig. 3 and discussion later). Finally, the term itself is also
unfortunate, implying that these traits somehow circumvent the normal processes of evolution. Therefore, we
suggest the more descriptive term, ‘multiple-effect trait’.
Multiple-effect traits shorten the TA chain, but may
not remove the need for TAs. When nonrandom mating
requires the evolution of more than one trait (e.g. signal-preference systems), direct selection acting on one
of them is not enough, and an association still has to
build up between these different traits (Fig. 3: B1a),
hence leaving some room for gene flow to allow recombination to slow down speciation. Moreover, direct
selection on signals is probably relatively inefficient in
producing reproductive isolation, as it requires evolution of the associated preferences, and indirect selection
on preferences is expected to be relatively weak:
females expressing those preferences do not immediately obtain fitness benefits from them and may incur
costs (Kirkpatrick & Barton 1997). Therefore, it appears
that multiple-effect traits, whose contribution to assortative mating is actually very weak, or which require
evolution at other traits for nonrandom mating to
evolve, may only increase the probability of speciation
marginally.
Servedio et al. (2011) distinguish ‘automatic magic
traits’ from ‘classic magic traits’ (of the type just
described which fit Fig. 3: B1a). Their automatic magic
traits correspond to exceptional cases, where there is no
need for any TA to be built among components of
reproductive isolation; they are multiple-effect traits,
which fit readily into our framework (length of the TA
chain = 0: Fig. 3: B2 and B3). Previous authors (Jiggins
et al. 2005; Wiley & Shaw 2010; Grace & Shaw 2011;
Merrill et al. 2011) have considered an allele under
direct selection, which pleiotropically influences both a
signal and a preference to be a ‘magic allele’ (Fig. 3:
B1b), but here, there is no single trait that has multiple
effects, and so there is always the possibility that new
alleles might influence just the signal or the preference
(Box 1). Environmentally induced trait divergence
might contribute to reproductive isolation in multiple
ways. For these reasons, we prefer to keep the focus on
multiple-effect traits rather than on genes or alleles. In
some cases, it may be difficult to distinguish between
a single multiple-effect trait and two traits that are closely connected functionally and have a strong tendency
to co-evolve (Box 1). However, it is not helpful to
extend the idea of multiple-effect traits to cases of very
close physical linkage between gene(s) influencing two
distinct traits (e.g. a habitat preference locus tightly
linked to a locally adapted trait locus or a preference
locus linked to a signal locus), because here, it is clear
that the two traits can evolve independently and each
new mutation will influence only one trait or the other.
In this respect, we differ from Servedio et al. (2011),
who consider magic traits to be encoded by magic
genes.
Multiple-effect traits can contribute to either oneallele or two-allele mechanisms. This is also clear from
our classification, where B3 (in Fig. 3) can be considered a multiple-effect version of the one-allele mechanism in A3, while B1 is the multiple-effect version of
A1. In this respect, we agree with Servedio et al. (2011).
Finally, we note that a trait may acquire multiple
effects on reproductive isolation. A polymorphism for
cryptic coloration may be under divergent selection
between habitats and have no effect on mating pattern.
However, if an allele spreads through the population
that causes individuals to choose the habitat in which
they are best camouflaged, then the coloration becomes
a multiple-effect trait, because it now influences both
survival and mating pattern. In conclusion, the comparative framework used here points to confusion about
the nature of traits that contribute to reproductive isolation in more than one way and allows us to clarify
what really constitute the most favourable scenarios for
speciation-with-gene-flow. While the recent literature
hypothesizes the existence of multiple-effect traits in an
increasing number of systems, cases where a single trait
is responsible for reproductive isolation may actually be
much rarer in nature (see Box 2 and Servedio et al.
2011).
Factors strengthening the links in the TA chain
With the exception of scenarios that do not require TAs
(Fig. 3: B2, B3) or otherwise avoid the need for LD
(Fig. 3: A3, B1b), the evolution of reproductive isolation
implies the establishment of TAs that typically rely on
some degree of LD, and therefore depends on factors
favouring the strengthening of LD in the face of gene
flow: physical linkage and reduced recombination
decrease the rate at which LD is broken up, strong
selection favours LD, migration increases LD within
subpopulations but also results in more heterozygous ⁄ hybrid genotypes, in which recombination can
reduce population-wide LD, and costs associated with
nonrandom mating can oppose the build-up of LD
between selected and mating loci (Gavrilets 2004). We
here review two mechanisms of current interest, as they
are hypothesised to favour the crucial associations that
promote isolation and protect them from the effects of
gene flow by reducing the effects of recombination.
The ‘recombination model’
The first hypothesis proposes that some regions of the
genome, particularly chromosomal inversions but also
2011 Blackwell Publishing Ltd
F R A M E W O R K F O R C O M P A R I N G P R O C E S S E S O F S P E C I A T I O N 11
centromeric regions, translocation break points and sex
chromosomes, are protected from recombination in
hybrids or heterozygotes, thus favouring the maintenance of differentiation and reproductive isolation,
despite gene flow (‘recombination model’, Butlin 2005).
In these regions, a reduction in actual recombination
rates is achieved through reduced pairing and crossing
over between inverted regions or by selection against
recombinant gametes. As a consequence, selection on
one or a few loci can reduce introgression for large
genomic regions, thus critically protecting favourable
genotypic combinations from being broken up by
recombination, including: local adaptation loci (Rieseberg 2001), intrinsic genetic incompatibilities in hybrids
(Noor et al. 2001) and LD between alleles conferring
adaptation and assortative mating (Butlin 2005). Extensions to these initial models have examined the role of
inversions in the initial build-up of genetic differences
between populations (Navarro & Barton 2003; Gavrilets
2004) and the factors driving the actual spread of inversions (Trickett & Butlin 1994; Kirkpatrick & Barton
2006; Feder et al. 2011).
Various lines of empirical data support these models:
rearrangements are detected in regions of lower genetic
divergence in co-occurring species than in allopatric
species; traits that prevent gene flow between species
preferentially map to rearranged regions of the genome;
and inverted regions tend to display higher genetic
divergence between species than noninverted regions
(Hoffmann & Rieseberg 2008). Similar observations
have been made in regions of restricted recombination
in proximity to centromeres (Butlin 2005). Moreover,
recent studies highlight the potential role of sex chromosomes in maintaining LD among ‘speciation genes’
(Kitano et al. 2009; Backstrom et al. 2010a,b; Dopman
et al. 2010; Pryke 2010). More recently, it has also been
shown that chromosomal inversions could favour the
birth and death of genes, therefore promoting adaptive
evolution (Furuta et al. 2011). Interestingly, a recent
study on the yellow monkeyflower Mimulus guttatus
demonstrated for the first time in nature the contribution of an inversion to adaptation and to multiple
reproductive isolating barriers (Lowry & Willis 2010),
thus documenting how such rearrangements can favour
LD among genes underlying reproductive isolation.
However, recent empirical studies also sometimes
contradict the importance of these specific genomic
regions by showing that regions of exceptionally high
differentiation are widely distributed across the genome
(Yatabe et al. 2007; Strasburg et al. 2009). Moreover,
inferring the role of restricted recombination from relative measures of divergence should be done with caution, as observed high interspecific differentiation can
sometimes result from segregation of ancestral variation
2011 Blackwell Publishing Ltd
or within-species processes, rather than from reduced
interspecific gene flow (Noor & Bennett 2009; White
et al. 2010).
‘Divergence hitchhiking’
In parallel, a recent hypothesis based on results
obtained in the pea aphid proposes a mechanism called
‘divergence hitchhiking’, by which genomic differentiation can be generated over large regions of the genome
in the early stages of ecological speciation as a consequence of disruptive selection, thus favouring progress
towards speciation (Via & West 2008; Via 2009). Previous theoretical work had already shed light on how
selection in subdivided populations can influence population differentiation at neutral loci: (i) local adaptation
in a heterogeneous environment because of disruptive
selection can result in substantial differences among
populations in the frequencies of neutral alleles closely
linked to selected loci because of their reduced effective
rate of gene flow (Charlesworth et al. 1997; Barton 2000;
but see Slatkin & Wiehe 1998; Santiago & Caballero
2005); (ii) the hitchhiking effect of an unconditionally
favourable mutation (directional selection) that spreads
from its deme of origin to other demes by migration
(‘hitchhiking in space’ Wiehe et al. 2005; or ‘global
hitch-hiking in a structured population’) can sometimes
generate peaks of differentiation at neutral loci (Slatkin
& Wiehe 1998; Santiago & Caballero 2005; Faure et al.
2008). Local hitchhiking may also contribute, where a
new allele spreads only through the habitat in which it
is advantageous (Morjan & Rieseberg 2004), and
increases the differentiation at closely linked neutral
loci. Although both local and global processes can generate high levels of neutral differentiation, only disruptive selection can potentially induce an association
between different components of reproductive isolation
by creating LD between adaptation loci and neutral loci
potentially involved in other barriers to gene flow
(Smadja et al. 2008). However, given the genomically
localised and transient properties usually described for
sweeps (Maynard Smith & Haigh 1974), can we really
expect disruptive selection to favour LD among components of reproductive isolation?
The hypothesis of divergence hitchhiking suggests
that the hitchhiking effect around loci under disruptive
selection is accentuated in comparison with intrapopulation situations, as local adaptation reduces the
effective interpopulation recombination rate (Via &
West 2008). In other words, the genetic barrier induced
by local adaptation should extend the zone of influence
of selection along the chromosome, and consequently,
loosely linked neutral loci could hitchhike to high
divergence. The bigger the effect of hitchhiking, the
12 C . M . S M A D J A and R . K . B U T L I N
Box 3 What about nongenetic factors?
Recent empirical and theoretical studies suggest a role for nongenetic mechanisms in promoting speciation-with-gene-flow.
Learning and early experience (imprinting) are being acknowledged as potential factors promoting
divergence, because they can increase the intensity of disruptive selection and strongly favour vertical
transmission of species-specific traits (therefore strengthening the TA chain) (Svensson et al. 2010).
Recent models suggest this for learned mate preference by sexual imprinting or learned habitat preference by ecological imprinting (Servedio et al. 2009; Stamps et al. 2009). Although learning can sometimes ease speciation in comparison with genetically inherited preferences, its influence strongly
depends on the degree to which cultural traits are properly imprinted or copied. In some cases, it can
also inhibit speciation if it promotes hybridisation or reduces the strength of selection. Mating traits,
such as bird songs that experience oblique imprinting, are more likely to promote signal divergence in
allopatry than in contact areas where mixed signals can be produced (Olofsson & Servedio 2008).
However, the still scarce empirical evidence seems to confirm a significant role, showing that speciation can be promoted by (i) sexual imprinting (fruit flies, Dukas 2008; guppies, Magurran & Ramnarine 2004; cichlids, Verzijden & ten Cate 2007; sticklebacks, Albert 2005), (ii) natal exposure to habitat
cues (e.g. host plant volatiles in Helicoverpa armigera, Li et al. 2005) or (iii) social imprinting (e.g. sticklebacks Kozak & Boughman 2008, 2009).
Similarly, phenotypic plasticity could facilitate speciation (Pfennig et al. 2010). Plasticity can permit
colonisation and persistence in novel environments, thus increasing the potential for future adaptive
genetic divergence (Crispo 2008). Because it allows a group of individuals to adapt simultaneously
without the need for standing genetic variation or for new mutations to arise, adaptation can potentially occur more rapidly via a plastic response than via genetic change. In effect, plasticity can reduce
the impact of gene flow on trait divergence and facilitate the evolution of TAs; for example, shifts in
flowering time can be at least partly plasticity-driven, and this plasticity for phenology being likely to
restrict gene flow between populations subject to divergent selection (Levin 2009). Convincingly, there
is evidence for accentuated differences between incipient species resulting from plastic phenotypic differentiation in some organisms (e.g. moth communication signals, Groot et al. 2009; morphological
divergence of Lake Victoria cichlid fish, Magalhaes et al. 2009; plastic host utilization in nymphalid
butterflies, Nylin & Janz 2009). However, a more comprehensive exploration is needed to draw general
conclusions, as plasticity can also potentially have the opposite effect when rapid phenotypic adaptation to new environmental conditions reduces the strength of divergent selection (Crispo 2008; Hendry
2009; Thibert-Plante & Hendry 2011).
Future research will have to show to what extent ‘cultural transmission’, phenotypic plasticity and
other nongenetic mechanisms (e.g. epigenetics) play a significant role in the evolution of reproductive
barriers in the face of gene flow.
more likely neutral loci underlying nonrandom mating
can take the lift, and the longer LD should persist over
time. Ultimately, divergence at nonrandom mating loci
will further reduce interpopulation gene flow and
provide a seed for divergence to be expanded over even
larger areas of chromosome. Theory suggests that when
population sizes are finite, the barrier at the selected
locus can modify the migration–drift equilibrium at
other loci, such that the differentiation does not vanish
completely, but remains stable at a higher level than the
differentiation of unlinked loci (Charlesworth et al.
1997; Bierne 2010; Feder & Nosil 2010). The homogeni-
sation of allele frequencies is, thus, slowed down by the
additional barrier to gene flow generated by the
selected locus, in proportion to linkage between the two
loci (Barton 1979). However, with larger populations,
differentiation via drift does not happen, thus reducing
the impact of selection on neighbouring sites (Bierne
2010; Feder & Nosil 2010; Thibert-Plante & Hendry
2010). Therefore, divergence hitchhiking could theoretically neutralise the challenge of generating and maintaining LD between selected and nonrandom mating
loci in the face of gene flow, but it may only apply to
restricted conditions, and further theoretical work is
2011 Blackwell Publishing Ltd
F R A M E W O R K F O R C O M P A R I N G P R O C E S S E S O F S P E C I A T I O N 13
needed to envisage how LD can spread among loosely
linked loci.
The hypothesis of divergence hitchhiking predicts
large regions of differentiation around selected loci.
What evidence do we have for this? In the pea aphid,
Via & West coupled QTL mapping and an AFLP scan
for selection to estimate the average size of the regions
affected by selection to be 20 centiMorgans (Via &
West 2008). They inferred from this estimation the presence of large genomic islands of differentiation (Turner
et al. 2005; Nosil et al. 2009a) consistent with divergence
hitchhiking. However, the method of genetic mapping
used in this study is biased towards finding a few
regions of large effect. Moreover, empirical evidence is
overall mixed: results in Coregonus whitefish are consistent with Via & West’s findings, but some studies
suggest much smaller genomic regions that are independent targets of selection (e.g. in Littorina snails (Wood
et al. 2008), Helianthus sunflowers (Scascitelli et al. 2010),
sticklebacks (Mäkinen et al. 2008) and Heliconius butterflies (Baxter et al. 2010)), while a recent study suggests
the existence of ‘continents’ of genomic differentiation
composed of multiple loci under selection rather than
isolated islands of differentiation (Michel et al. 2010).
The efficacy of this mechanism in promoting speciation
depends on the size of the region affected by divergence
hitchhiking, and future work should focus on the extent
to which regions of divergence that are generated can
‘grow’ during the speciation process, and the significance of such growth for causing reduced gene flow
between incipient species. In parallel, the increasing
availability of whole-genome re-sequencing and scans
for differentiation to many more researchers and projects (Burke et al. 2010) should rapidly shed light on the
dynamics and architecture of genomic differentiation all
through the speciation process.
The picture of the possible mechanisms favouring the
evolution and maintenance of LD, and so the strengthening of the TA chain, is not completed yet, but these
recent contributions show that insights into the detailed
mechanisms underlying speciation-with-gene-flow are
within reach. Assessing the significance of the proposed
mechanisms is a crucial avenue for future refined
empirical studies and additional theoretical developments.
Concluding remarks and future directions
Speciation with gene flow is most likely where the TA
chain required for the evolution of reproductive
isolation is short. Where TAs are required, pleiotropy
can significantly enhance the probability of speciation.
Nevertheless, the coupling together among the different
components of reproductive isolation is crucial for
2011 Blackwell Publishing Ltd
many scenarios of speciation-with-gene-flow, and in
most cases, it relies on the build-up of linkage disequilibrium among genes underlying the component isolating barriers. This provides a framework in which
models or empirical examples of speciation with gene
flow can be compared fruitfully on the basis of the
length of the TA chain and the factors that promote
associations where they are required. We have highlighted the importance of genetic factors in promoting
divergence under these constrained conditions, and one
important avenue for future research is to further
explore and characterise these genetic drivers, in particular by taking advantage of new developments in
genomics and high-throughput technologies (Rice et al.
2011). However, there is also an increasing appreciation
of the possible role of nongenetic mechanisms (e.g.
learning, imprinting, phenotypic plasticity, epigenetics)
in favouring divergence between populations experiencing gene flow (Box 3). This is one further reason to
focus first on TAs and upcoming research if likely to
focus further on these potentially important nongenetic
factors. However, it is important to note here that not
only do we need to identify potential factors favouring
divergence in the presence of gene flow but we also
need to test whether they actually promoted divergence
in nature (Hendry 2009; Nosil & Schluter 2011).
Reviewing and comparing factors influencing divergence-with-gene-flow under this comparative framework also enabled us to extract the situations most
favourable to speciation-with-gene-flow: for example,
the cases that minimise TAs, including ‘one-allele’ scenarios and multiple-effect traits (Fig. 3: A3, B2, B3).
Recent enthusiasm for the role of multiple-effect traits
has led to a need for clarification of the different possible mechanisms involved (‘automatic’ and ‘classic’
magic traits; Servedio et al. 2011). The more complete
framework we propose readily incorporates these
mechanisms and should provide the grounding for a
more robust comparative exploration of the conditions
associated with speciation-with-gene-flow in nature.
Highlighting the general conditions favouring speciation-with-gene-flow is an important step towards
getting a more integrated view of the mechanisms
underlying divergence, and the framework identified
here will provide the basis for further comparative
analysis that will help to gain insights into the
conditions and the combinations of factors, under
which speciation-with-gene-flow most frequently
occurs in nature.
Acknowledgements
We thank the three anonymous referees and the editor, Louis
Bernatchez, for their useful comments. We also thank Mike
14 C . M . S M A D J A and R . K . B U T L I N
Ritchie, Maria Servedio, Patrik Nosil, Sara Via, Mohamed
Noor, Jon Slate and Jessica Stapley for their comments on an
earlier version of the manuscript, and Martine Maan and Chris
Jiggins for fruitful discussions on ‘magic’ speciation. CS
acknowledges the Centre National de la Recherche Scientifique
(CNRS), and RB acknowledges NERC for financial support.
This is publication ISEM no. 2011-130.
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