invited review a framework for comparing processes of ... · invited review a framework for...

Molecular Ecology (2011) doi: 10.1111/j.1365-294X.2011.05350.x

INVITED REVIEW

A framework for comparing processes of speciationin the presence of gene flow

CAROLE M. SMADJA* and ROGER K. BUTLIN†

*Centre National de la Recherche Scientifique (CNRS), Institut des Sciences de l’Evolution UMR 5554, cc065 Universite

Montpellier 2, 34095 Montpellier, France, †Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10

2TN, UK

Corresponde

E-mail: carol

� 2011 Black

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-with-

gene-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 sepa-

ration or in secondary contact zones is a plausible route

to speciation (Servedio & Noor 2003; Bolnick & Fitzpa-

trick 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 ‘diver-

gence-with-gene-flow’ or ‘speciation-with-gene-flow’

(Rice & Hostert 1993) has been spreading in the litera-

ture, reflecting interest in a more continuous vision of

speciation in time and space (Butlin et al. 2008; Fitzpa-

trick 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

nce: Carole Smadja, Fax: +33(0)467143622;

[email protected]

well 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 diver-

gence in the face of gene flow such as reinforcement

(Servedio & Noor 2003; Ortiz-Barrientos et al. 2009;

Servedio 2009) or sympatric speciation (Bolnick & Fitz-

patrick 2007; Fitzpatrick et al. 2008, 2009), the role of

selection (Kirkpatrick & Ravigne 2002; Dieckmann et al.

2004; Gavrilets 2004; Maan & Seehausen 2011) or more

specifically ecologically driven selection (ecological spe-

ciation 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 pre-

vious reviews and considering more recent advances,

we take a broader look at the mechanisms favouring

speciation-with-gene-flow to extract the essential fea-

tures 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 LI 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 (Gavri-

lets 2004), but does not exclude nonadaptive mecha-

Fig. 1 Speciation-with-gene-flow in context. The figure distinguishes

populations (left of dashed line) from those with geographical or eco

dashed line). The different types of evolutionary and selective force

define and delimit different modes and mechanisms of speciation (co

nisms (Rundell & Price 2009); second, it includes cases

of ecological speciation (green frame) and more gener-

ally 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 sec-

ondary contact, but excludes cases of instantaneous spe-

ciation in sympatry, where no gene flow opposes

divergence (grey frame). This picture provides addi-

tional arguments against categorising speciation (Butlin

et al. 2008), as it underlines the fact that many catego-

ries 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.

scenarios of speciation with no contact at all between diverging

logical contact at least at some point in time and space (right of

s potentially involved in each scenario (grey text) are used to

loured frames).

� 2011 Blackwell Publishing Ltd

(a)

(b)

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 pro-

cess, 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 cur-

rently share part or all of their distribution ranges, cur-

rently 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 varia-

tion pre-dating speciation may be mistaken for a signa-

ture 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 distri-

butions of gene flow parameters, given patterns in

nucleic acid sequences, and have inferred that specia-

tion 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 concur-

rent 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.

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 sev-

eral 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 com-

ponents of reproductive isolation.

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 & Ravigne 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


& Tautz 2010); allow genetic variants from different

populations to come together in a single population, up

to and including the generation of reproductively iso-

lated 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 segrega-

tion (Felsenstein 1981)(we will hereafter refer to ‘recom-

bination’ as a shortcut for ‘recombination and

segregation’). Therefore, the challenge lies in under-

standing the factors favouring the evolution of repro-

ductive isolation, despite these two effects of gene flow.

Gavrilets and colleagues have shown how mathematical

models can provide great insights into the potential fac-

tors 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 specia-

tion process and the potential conditions that may


favour divergence, and we define a general framework

within which the likelihood of divergence-with-gene-

flow 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 con-

tributing to different reproductive barriers) (Coyne &

Orr 2004; (Fig. 2a). Speciation depends on the availabil-

ity of suitable genetic variation in the traits underlying

reproductive isolation (Barrett & Schluter 2008), and it

may involve divergence in these traits between subpop-

ulations and commonly progresses towards complete

Box 1 Pleiotropy, traits and effects

Pleiotropy is the situation where ‘one allele affects tw

definition is important for discussions of the role of

of an allele, not of a gene. It is possible for one alle

while others influence only one of the traits, or ne

Servedio et al. 2011) is potentially misleading. Similar

effects on two traits does not necessarily mean that o

have pleiotropic effects. The term ‘pleiotropic trait

avoided.

A clear terminology is available from quantitative g

notype relationships. Correlations between traits at

underlying genetic correlations, and these correlatio

partly to linkage disequilibrium (Falconer & Mackay 1

There are some pairs of traits that necessarily shar

physiological architecture. An example might be male

tic signal and female preference that share a common

such traits, pleiotropy will be common. Nevertheless,

independently by genetic or environmental changes

pleiotropy’ (Fig. 3). They are clearly part of a contin

nistic links will evolve more easily than pairs with few

facilitate speciation.

We also emphasise the distinction between traits an

ple. This trait may influence both survival and repr

mating success with females that have preferences for

fitness and on nonrandom mating. Through both ro

Although there are multiple effects, there is only a sin

this situation with pleiotropy, although others have

2005). Keeping to a precise definition of pleiotropy, s

the genetic and environmental effects that generate

and their effects, helps to clarify the nature of the TA

Box 2).

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

o or more traits’ (Barton et al. 2007). This precise

pleiotropy in speciation. Pleiotropy is a property

lic substitution in a gene to influence two traits,

ither. Thus, referring to ‘pleiotropic genes’ (e.g.

ly, the fact that a particular allele has pleiotropic

ther alleles at the same or at other loci will also

’ (e.g. Jiggins et al. 2005) should, therefore, be

enetics to deal with multiple-gene, multiple-phe-

the phenotypic level may be partly because of

ns in turn are partly because of pleiotropy and

996).

e a significant part of their underlying genetic or

and female body size, or perhaps a male acous-

underlying oscillator (Butlin & Ritchie 1989). For

it is perfectly possible for them to be influenced

. We refer to these cases as showing ‘extensive

uum, but TAs between pairs with strong mecha-

er underlying connections. As a result, they will

d their effects. Take male tail length as an exam-

oductive success in different environments and

long or short tails. The single trait has effects on

utes it may contribute to reproductive isolation.

gle trait. We feel that it is not helpful to conflate

done so (e.g. ‘pleiotropic effects’ in Jiggins et al.

eparating discussion of traits from discussion of

trait variation, and distinguishing between traits

chain underlying speciation (see main text and


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 adapta-

tion 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 Leon et al. 2010); body size in sticklebacks (McKin-

non & 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 contribu-

tions 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 exam-

ples 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 sig-

nal 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 associa-

tion 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).

The pea aphid, Acyrthosiphon pisum. Image Credit: Shipher Wu

(photograph) and Gee-way Lin (aphid provision), National Tai-

wan University, from http://dx.doi.org/10.1371/image.pbio.

v08.i02.g001.Heliconius cydno (white) and H. pachinus (yellow). Image Credit:

Marcus R. Kronforst, Harvard University.



Probably, the best examples of multiple-effect traits with strong contributions to reproductive isola-

tion 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 evolv-

ing 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 disrupt-

ing associations previously formed in allopatry. This is

why forming the connection between the different com-

ponents of reproductive isolation represents the princi-

pal challenge in many scenarios of speciation-with-

gene-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 counter-

acts the deleterious effect of recombination on LD will

favour speciation.

We note that genome-wide LD is a signature of speci-

ation, 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, associa-

tions 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 selec-

tion 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 isolationin 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-


Type of prezygotic isolating mechanism The TA chain Minimum numberof TA

Minimum levels of LD

Divergence required?

Opposed by gene flow via..

A- Indirect selection on non-random mating traits Post-zygotic isolation components

Prezygotic isolation components

1a- Signal-preference signal preference 2 2 Yes Dilution/ recombination

1b- Extensive pleiotropy between signal & preference

2 1 Yes Dilution/ recombination

2- Single trait (e.g.flowering time, habitat preference, assortment trait)

1 1 Yes Dilution/ recombination

3- One-allele(e.g. no migration or assortment allele)

1 0 Yes Dilution

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 compo-

nents of reproductive isolation, the fewer the opportu-

nities that gene flow will have to oppose divergence

or to breakdown the coupling between components of

reproductive isolation, and therefore the easier specia-

tion 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 associa-

tion 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,


through linkage disequilibrium, the different compo-

nents 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 recombi-

nation (e.g. Kirkpatrick & Barton 2006). In the next

sections, we use the combination of these two ingredi-

ents as a framework for reviewing the factors favour-

ing speciation-with-gene-flow.

Factors influencing the length of the traitassociation 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


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 com-

monly requires a trait under divergent selection to

become associated with a source of prezygotic isolation,

which is the ultimate step for most speciation-with-gene-

flow scenarios (Kirkpatrick & Ravigne 2002; Gavrilets

2004; Servedio 2009). How the type of prezygotic isolat-

ing 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 sig-

nal 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 diver-

gence 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 specia-

tion 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 sub-

populations (Fig. 3: B2) has a long history (Maynard

Smith 1966: ‘pleiotropy model’, Gavrilets 2004: ‘similar-

ity-based’ non-random mating). Flowering time is, per-

haps, 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, espe-

cially 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 exam-

ple, 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 habi-

tats (Fig. 3: A3). This is equivalent to the assortative

mating model of Servedio (2000), where divergent selec-

tion 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 subpopula-

tions, 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 pro-

gress towards speciation.

An assortative mating trait like flowering time may

not be under direct selection, but progress towards spe-

ciation 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 em-

phasises how reinforcement can involve different

lengths of TA chain. Speciation is likely to be most con-

strained where assortative mating results from the oper-



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 selec-

tion may be divergent or disruptive ecological selection

(resulting in extrinsic postzygotic isolation and ⁄ or com-

ponents of prezygotic isolation such as immigrant invia-

bility, Nosil et al. 2005), or it may be the result of

intrinsic incompatibilities, especially following second-

ary 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 an-

droconia on butterfly wings may also influence mate

choice. Here, the trait under direct selection, colour pat-

tern, is distinct from the signal trait. This case fits sce-

nario 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 mat-

ing traits along with LD between loci that influence

only colour or pheromones.

Overall, this comparison highlights the possible varia-

tion 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


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 speciation-

with-gene-flow more likely.

We note that history can be an additional determi-

nant 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 by-

product 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 influ-

ences more than one component of reproductive isola-

tion (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 combi-

nations 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 cockcha-

fers and probably other insects (Ruther et al. 2000; Es-

trada & 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 require-

ments for LD, is too great to be encompassed by a sim-

ple magic vs. nonmagic distinction. Moreover, the use of

the term ‘magic trait’ can misleadingly imply that specia-

tion itself becomes automatic or inevitable where such

traits are involved, which is not true in most cases (see


Fig. 3 and discussion later). Finally, the term itself is also

unfortunate, implying that these traits somehow circum-

vent 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. sig-

nal-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 recom-

bination to slow down speciation. Moreover, direct

selection on signals is probably relatively inefficient in

producing reproductive isolation, as it requires evolu-

tion of the associated preferences, and indirect selection

on preferences is expected to be relatively weak:

females expressing those preferences do not immedi-

ately obtain fitness benefits from them and may incur

costs (Kirkpatrick & Barton 1997). Therefore, it appears

that multiple-effect traits, whose contribution to assorta-

tive 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 clo-

sely 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 one-

allele or two-allele mechanisms. This is also clear from

our classification, where B3 (in Fig. 3) can be consid-

ered a multiple-effect version of the one-allele mecha-

nism 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 compar-

ative framework used here points to confusion about

the nature of traits that contribute to reproductive isola-

tion 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 heterozy-

gous ⁄ 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



centromeric regions, translocation break points and sex

chromosomes, are protected from recombination in

hybrids or heterozygotes, thus favouring the mainte-

nance 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 (Riese-

berg 2001), intrinsic genetic incompatibilities in hybrids

(Noor et al. 2001) and LD between alleles conferring

adaptation and assortative mating (Butlin 2005). Exten-

sions 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 inver-

sions (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 chro-

mosomes 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 contribu-

tion 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 rela-

tive measures of divergence should be done with cau-

tion, as observed high interspecific differentiation can

sometimes result from segregation of ancestral variation


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 differentia-

tion can be generated over large regions of the genome

in the early stages of ecological speciation as a conse-

quence of disruptive selection, thus favouring progress

towards speciation (Via & West 2008; Via 2009). Previ-

ous theoretical work had already shed light on how

selection in subdivided populations can influence popu-

lation 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 gen-

erate high levels of neutral differentiation, only disrup-

tive 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 compo-

nents of reproductive isolation?

The hypothesis of divergence hitchhiking suggests

that the hitchhiking effect around loci under disruptive

selection is accentuated in comparison with intra-

population 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

Box 3 What about nongenetic factors?

Recent empirical and theoretical studies suggest a role for nongenetic mechanisms in promoting speci-

ation-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 prefer-

ence by ecological imprinting (Servedio et al. 2009; Stamps et al. 2009). Although learning can some-

times 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 specia-

tion can be promoted by (i) sexual imprinting (fruit flies, Dukas 2008; guppies, Magurran & Ramnar-

ine 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. stick-

lebacks 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 poten-

tially 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 dif-

ferentiation 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 adapta-

tion 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 theoreti-

cally neutralise the challenge of generating and main-

taining 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



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 pres-

ence 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 consis-

tent with Via & West’s findings, but some studies

suggest much smaller genomic regions that are indepen-

dent targets of selection (e.g. in Littorina snails (Wood

et al. 2008), Helianthus sunflowers (Scascitelli et al. 2010),

sticklebacks (Makinen et al. 2008) and Heliconius butter-

flies (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 signifi-

cance 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 pro-

jects (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 strength-

ening 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 develop-

ments.

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


many scenarios of speciation-with-gene-flow, and in

most cases, it relies on the build-up of linkage disequi-

librium among genes underlying the component isolat-

ing 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 high-

lighted 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 partic-

ular 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 experienc-

ing 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 diver-

gence-with-gene-flow under this comparative frame-

work also enabled us to extract the situations most

favourable to speciation-with-gene-flow: for example,

the cases that minimise TAs, including ‘one-allele’ sce-

narios 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 possi-

ble 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 specia-

tion-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


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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C.S. and R.B. are evolutionary biologists primarily interested in

speciation.


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