Abstract

Reinforcement—the process whereby maladaptive hybridization leads to the strengthening of prezygotic isolation between species—has a long history in the study of speciation. Because reinforcement affects traits involved in mate choice and fertility, it can have indirect effects on reproductive isolation between populations within species. Here we review examples of these “cascading effects of reinforcement” (CER) and discuss different mechanisms through which they can arise. We discuss three factors that are predicted to influence the potential occurrence of CER: rates of gene flow among populations, the strength of selection acting on the traits involved in reinforcement, and the genetic basis of those traits. We suggest that CER is likely if (1) the rate of gene flow between conspecific populations is low; (2) divergent selection acts on phenotypes involved in reinforcement between sympatric and allopatric populations; and (3) the genetic response to reinforcement differs among conspecific populations subject to parallel reinforcing selection. Future work continuing to address gene flow, selection, and the genetic basis of the traits involved in the reinforcement will help develop a better understanding of reinforcement as a process driving the production of species diversity, both directly and incidentally.

Introduction: Speciation, Reinforcement, and Reproductive Character Displacement

Speciation is the evolutionary process by which one lineage splits into two reproductively isolated groups of organisms ( Coyne and Orr 2004 ). As such, a central goal of speciation research is to understand the processes that drive the evolution of reproductive isolation between different populations or species ( Darwin 1859 ; Dobzhansky 1940 ; Coyne and Orr 1989 , 2004 ; Nosil 2012 ). Significant strides have been made towards identifying barriers that generate reproductive isolation between species (hereafter referred to as “isolating barriers” or “barriers”; Coyne and Orr 2004 ; Harrison 2012 ), the processes underlying their evolution ( Dobzhansky 1937 ; Liou and Price 1994 ; Noor 1995 ; Rundle and Nosil 2005 ; Seehausen et al . 2008 ; Maan and Seehausen 2011 ), and the rate at which they evolve during speciation ( Coyne and Orr 1989 , 1997 ; Bolnick and Near 2005 ; Moyle and Nakazato 2010 ; Matute et al . 2010 ).

Barriers to reproduction can be classified depending on where they occur in the reproductive cycle of an organism. Prezygotic barriers occur before the zygote is formed and can be further split into premating and postmating-prezygotic barriers. Premating barriers include ecological and behavioral traits that reduce the likelihood that two individuals will mate, whereas postmating-prezygotic barriers involve interactions between gametes or between sperm and aspects of female reproductive tracts. Finally, postzygotic barriers occur after fertilization, and include any reduction in fitness observed in hybrid organisms.

During speciation, premating barriers are thought to be crucial. Comparative studies have found that premating reproductive isolation evolves faster than postzygotic isolation in areas where species can interbreed ( Coyne and Orr 1989 , 1997 ; Yukilevich 2012 ). Additional phylogenetic studies have shown that the rate of evolution of premating barriers is also comparatively faster than that of postzygotic traits ( Coyne and Orr 1989 ; Yukilevich 2012 ; Rabosky and Matute 2013 ), which has led to the hypothesis that premating traits are the first type of reproductive barriers to evolve to substantially high levels and thus are crucial to the process of speciation. The processes that lead to the evolution of strong premating barriers may therefore be fundamental in generating and maintaining biological diversity ( Noor 1999 ; Kay and Schemske 2008 ; Hudson and Price 2014 ).

One process that can drive the evolution of premating barriers is selection either against the formation of maladapted hybrids ( Dobzhansky 1940 ) or against negative fitness effects of hybrid matings on females ( Lorch and Servedio 2007 ). In this process—referred to as reinforcement—indirect selection against maladaptive hybridization results in the evolution of strong prezygotic isolating barriers between individuals of two species in regions where those species co-occur (i.e., sympatry; Dobzhansky 1937 , 1940 ). Reinforcement frequently generates a pattern of reproductive character displacement (RCD; Brown and Wilson 1956 ), where prezygotic isolation between two hybridizing species is stronger in sympatry when compared with allopatry [see Servedio and Noor (2003) for other patterns generated by reinforcement). Although the importance of reinforcement has been hotly debated ( Templeton 1981 ; Spencer et al . 1986 ; Butlin 1987 ; Sanderson 1989 ), an increasing amount of empirical and theoretical support suggests that it may be a widespread and important process during speciation, capable of promoting the evolution of prezygotic isolation ( Koopman 1950 ; Liou and Price 1994 ; Noor 1995 ; Servedio and Noor 2003 ; Nosil et al . 2003 ; Kay and Schemske 2008 ; Matute 2010 ; Yukilevich 2012 ; Hudson and Price 2014 ).

Reinforcement and the Evolution of Incidental Reproductive Isolation among Conspecific Populations

Reinforcement results in a decrease in the likelihood of maladaptive matings through the evolution of phenotypes that are involved in mate recognition, mate choice, and/or gametic compatibility (i.e., prezygotic traits). When the evolutionary response to reinforcement causes phenotypes to become “mismatched” between populations of the same species, reproductive isolation can evolve between those populations as an incidental effect of reinforcement ( Howard 1993 ; Pfennig and Ryan 2006 ; Ortiz-Barrientos et al . 2009 ; Hoskin and Higgie 2010 ; Abbott et al . 2013 ). Here, we refer to these effects as the “cascading effects of reinforcement” (CER). The evolutionary consequences of CER differ from those of reinforcement because the former occur between conspecific populations whereas the latter occur between species. The idea that reinforcement can have incidental effects on levels of reproductive isolation between conspecific populations was initially verbalized in the late 1960s ( Littlejohn and Loftus-Hills 1968 ). Nonetheless, this idea was only recently formally put forth in the literature ( Howard 1993 ; Ortiz-Barrientos et al . 2009 ; Hoskin and Higgie 2010 ), and it has rarely been tested from a theoretical perspective (however, see Pfennig and Ryan 2006 ). Below, we summarize two general mechanisms through which reinforcing selection can lead to the incidental evolution of reproductive isolation between conspecific populations and propose a route map for its study.

CER caused by parallel reinforcing selection acting within multiple conspecific populations

The first mechanism that can lead to CER occurs when parallel reinforcing selection, acting within multiple populations of the same species ( Abbott et al. 2013 ; Figure 1 A), results in the convergent evolution of reinforced reproductive isolation (RRI). There are two possible outcomes to parallel reinforcing selection acting within conspecific populations. First, these populations can evolve RRI by responding to selection through the use of the same phenotypes and underlying loci. We do not consider this outcome a CER because the response to reinforcing selection is not expected to generate reproductive isolation between conspecific populations. Second, reinforcement can drive convergent evolution through different traits, phenotypes, and/or loci in the different populations. In this second outcome, reinforcement can lead to phenotypic differentiation between populations, which in turn can lead to reproductive isolation. Hereafter we refer to the effects of this type of CER as convergent-sympatry (c-s) effects ( Figure 1 A).

Figure 1.

Cascading effects of reinforcement that generate reproductive isolation (RI) among conspecific populations. (A) C-s effects are the result of reinforcing selection acting in multiple, geographically isolated populations of the same species. The response to reinforcing selection in these populations can differ (as indicated by the gray arrows showing shifts in phenotypes) and this can in turn lead to reproductive isolation. The word “phenotype” in the bottom histograms could have just the same been replaced with “genotype”. (B) S–a effects arise between populations undergoing reinforcement (dark gray box) and those found in allopatry (light gray box). In one scenario, if reinforcing selection causes phenotypes favored in sympatry to be disadvantageous in allopatry, reinforcement can lead to reproductive isolation between sympatric and allopatric populations. See text for further scenarios and descriptions.

Figure 1.

Cascading effects of reinforcement that generate reproductive isolation (RI) among conspecific populations. (A) C-s effects are the result of reinforcing selection acting in multiple, geographically isolated populations of the same species. The response to reinforcing selection in these populations can differ (as indicated by the gray arrows showing shifts in phenotypes) and this can in turn lead to reproductive isolation. The word “phenotype” in the bottom histograms could have just the same been replaced with “genotype”. (B) S–a effects arise between populations undergoing reinforcement (dark gray box) and those found in allopatry (light gray box). In one scenario, if reinforcing selection causes phenotypes favored in sympatry to be disadvantageous in allopatry, reinforcement can lead to reproductive isolation between sympatric and allopatric populations. See text for further scenarios and descriptions.

C-s effects constitute an example of a mutation order process ( Mani and Clarke 1990 ). Mutation order processes occur when adaptation to similar selective environments (e.g., in populations experiencing parallel reinforcing selection) utilize different genetic or phenotypic pathways due to the stochastic effects of mutation, substitution, and/or the available pool of standing genetic variation ( Schluter 2009 ). Theoretical work has shown that differentiation through mutation order processes (and by extrapolation, c-s effects) is most likely to occur in scenarios where rates of gene flow between conspecific populations are low, as this allows populations to evolve and maintain genetic and phenotypic differences ( Nosil and Flaxman 2011 ).

C-s effects can result in prezygotic isolation, postzygotic isolation, or both evolving between conspecific populations. If mutation order processes resulting from c-s effects lead to prezygotic isolation without any postzygotic isolation, then such differentiation falls into the category of an incidental effect of reinforcement (i.e., a c-s effect). However, mutation order processes could also cause postzygotic isolation through the substitution of different, and incompatible, alleles in different conspecific populations undergoing reinforcement. In this case, mating between conspecific populations would become maladaptive, and reinforcement sensu stricto could cascade to populations of the same species. Prezygotic isolation could then evolve as the direct result of reinforcement (i.e., selection against the maladaptive consequences of postzygotic isolation), and the presence of postzygotic isolation would have been an incidental effect of reinforcement that was initially acting independently in parallel populations of the same species. The largest difficulty in identifying c-s effects (as we see it) will be one’s ability to causally ascribe parallel reinforcing selection as the mechanism driving the differentiation of conspecific traits.

As one of the few putative examples of a c-s effect, Lemmon (2009) quantified differences in acoustic signals (mating calls) among four populations of the chorus frog Pseudacris feriarum undergoing RCD in sympatry with the heterospecific P. nigrata . In different regions of sympatry, pulse number and pulse rate of P. feriarium calls differ from P. nigrata calls. More importantly, the sympatric P. feriarium calls also differ from one another. Parallel reinforcing selection has therefore resulted in the diversification of call types among populations of P. feriarum . While reproductive isolation between conspecific populations of P. feriarum was not explicitly tested in this study, this case may constitute (incipient) mutation order speciation if the differences in conspecific calls lead to reproductive isolation between conspecific populations. This example highlights how the same selective pressure—namely selection against maladaptive hybridization in sympatry—can lead to the incidental differentiation, and diversification, of conspecific traits.

CER caused by divergent selection acting between conspecific populations undergoing reinforcement and those found in allopatry

The most common (or at least detectable) signature of reinforcement is RCD ( Howard 1993 ; Lemmon et al . 2004 ). However, the factors that generate or maintain RCD among conspecific populations are frequently unknown. For example, RCD can arise as a result of geographic isolation that exists between populations of a species undergoing reinforcement or divergent selection acting on the phenotype(s) involved in reinforcement between sympatric and allopatric regions of a species’ range ( Higgie et al . 2000 ; Hopkins et al . 2014 ; Pfennig and Rice 2014 ). Here we focus on the latter of these two mechanisms because divergent selection can result from the action of reinforcement, whereas geographic isolation can be due to other ecological or environmental factors.

Selection acting against phenotypes favored by reinforcing selection in allopatric regions of a species’ range can generate divergent selection on those phenotypes and can drive RCD ( Walker 1974 ; Price and Liou 1994). Here, we collectively refer to the effects caused by divergent selection between sympatry and allopatry as “sympatry–allopatry” or “s–a” effects ( Figure 1 B). S–a effects can manifest as a result of selection acting directly against reinforced phenotypes in allopatry ( Hopkins et al . 2014 ) or against pleiotropic or correlated phenotypes that have evolved with the reinforced phenotypes ( Comeault et al . 2015 ). The Texas wildflower Phlox drummondii provides a good example of a system where a reinforced phenotype is directly selected against in allopatric regions of the species’ range. Hopkins et al . (2014) showed that P. drummondii with red colored flowers are favored by reinforcing selection in regions where P. drummondii co-occurs with the blue-flowered species P. cuspidata . Blue flowers, on the other hand, are favored in allopatric regions of P. drummondii ’s range. Clines in flower color have been used to show that divergent selection limits the spread of different colored flowers (and their underlying alleles) between sympatric and allopatric regions of P. drummondii ’s range ( Hopkins and Rausher 2014 ). This example represents an s–a effect of reinforcement because reinforcement has led to the diversification of flower color in P. drummondii and this phenotypic diversification is predicted to generate selection against migrants (a form of reproductive isolation) between allopatric and sympatric regions of P. drummondii ’s range.

S–a effects can also occur when reinforcement indirectly drives the evolution of traits or phenotypes that are correlated with those undergoing reinforcement. This can occur through genetic linkage or additive genetic co-variation between traits. An example of this type of indirect cost has been observed in the fruit fly Drosophila yakuba . Female D. yakuba that are sympatric with their sister species D. santomea show evidence for reinforcement and lay fewer eggs when mated to male D. santomea than allopatric females. In addition to this female trait, male D. yakuba collected from sympatric populations have lower fertility when mated to conspecific females from allopatric populations ( Comeault et al . 2015 ). Comeault et al. (2015) used experimental evolution to show that this s–a effect is likely the result of a correlated evolutionary response in male gametes due to reinforcing selection that acts on an unidentified trait in the female reproductive tract. These results show how reinforcing selection acting on females can drive a correlated evolutionary response in male traits that are selected against in allopatry.

In general, s–a effects of reinforcement have received more attention in the literature than c-s effects. Table 1 highlights this and, to our knowledge, only three of the examples in this table suggest that c-s effects could be occurring: those of the stick insect Timema cristinae ( Nosil et al. 2003 ), the chorus frog P.feriarum ( Lemmon 2009 ), and the killifish Lucania parva ( Kozak et al . 2015 ). However, c-s and s–a effects are not mutually exclusive. In the chorus frog P. feriarum , for example, c-s effects are the result of acoustic signal traits that are favored by reinforcement but are predicted to increase the energetic cost of signaling relative to allopatric signal types ( Lemmon 2009 ). Energetic costs such as these could result in selection against reinforced signal phenotypes in allopatry. If this were the case, then parallel divergence in these traits (i.e., c-s effects) would also result in s–a effects. In order to fully appreciate the diversity and frequency of CER, research will need to continue to identify the phenotypes involved in reinforcement and determine how they are favored (or disfavored) by selection across a species’ range.

Table 1.

Systems where cascading effects of reinforcement have been implicated in within species differentiation

Species Trait Selection Gene flow? Genetic basis References 
Drosophila serrata Male cuticular hydrocarbons (CHCs) have diverged between sympatric and allopatric populations. Female preference is based on CHCs and has also diverged. Divergent natural between sympatry and allopatry. Sexual selection opposes reinforcing selection Unknown Differences in cuticular hydrocarbon profiles are explained by a few loci of large effect; one known locus: mFAS (12–30% of PV) Higgie et al. (2000) ; Higgie and Blows (2008) ; Hine et al. (2011) ; Chung et al. (2014) 
Drosophila mojavensis Female preferences differ between sympatric and allopatric populations. Male CHCs are hypothesized to have diverged as well. Unknown  Moderate to high among populations of D. mojavensis. Early in the divergence between D. arizonae and D. mojavensis Hypothesized to be mono- or oligogenic. Male and female courtship behaviors might be under the control of separate alleles or sex-specific behaviors are controlled by the same gene or genes acting in a sex-specific manner. The specific details remain unknown Wasserman and Koepfer (1977) ; Zouros and D’Entremont (1980) ; Markow (1991) ; Massie and Markow (2005) ; Ross and Markow (2006) ; Lohse et al . (2015) ,Jennings and Etges 2010 
Drosophila subquinaria Both male and female CHCs differ between sympatric and allopatric populations. Clines in mate discrimination and genetic markers suggest reinforcing selection is advantageous only in sympatry Reduced gene flow inferred from clines, but not directly measured. Unknown  Jaenike et al . (2006) ; Curtis et al . (2013) ; Giglio and Dyer (2013) ; Bewick and Dyer (2014) ; Dyer et al . (2014)  
Drosophila yakuba Gametic incompatibility between sympatric and allopatric populations. Female traits involved in retention or use of sperm. Clines in gametic isolation suggest reinforcing selection is advantageous only in sympatry. Mitochondrial introgression in the São Tomé hybrid zone. Moderate evidence of nuclear introgression between species and extensive gene flow between allopatric and sympatric lines Unknown Llopart et al. (2005) ; Bachtrog et al. (2008) ; Beck et al. (2015) 
Litoria verreauxii Male call differs between sympatric and allopatric populations. Unknown Unknown Unknown Littlejohn and Loftus-Hills (1968) 
Lucania parva Unknown, but potentially linked to body length and size of anal fin Unknown Unknown Unknown Kozak et al. (2015) 
Pseudacris feriarum Male call and female preference differ among multiple hybrid zones Not measured, but aspects of mating signal favored in sympatry might be costly in allopatry. Possible case of convergent reinforcing selection Unknown Unknown Lemmon (2009) 
Litoria genimaculata Male call differs among populations. Individuals from contact zones are discriminated upon by allopatric individuals Unknown Unknown Hoskin et al. (2005) 
Spea multiplicata  Male call and female choice have evolved via reinforcement in areas where S. bombifrons is present  Unknown  Gene flow is slightly reduced among sympatric and allopatric populations. No information of gene flow between S. multiplicata and S. bombifrons Unknown Pfennig and Simovich (2002) ; Pfennig and Pfennig (2005) ; Pfennig and Rice (2014) 
Gryllus fultoni Calling song/female preference Not measured yet, but females prefer local song types. Possible case of a one-allele mechanism Unknown Unknown Jang and Gerhardt (2006a , b )  
Magicicada neotredecim Calling song/female preference Not measured, but females prefer local song types. Possible case of a one-allele discrimination model Unknown Unknown  Cooley et al . (2006)  
Phlox drumondii  Flower color and hue have evolved under reinforcing selection in areas where P. cuspidata is also present. Reproductive isolation between red and blue morphs of P. drumondii driven by selection against migrants . Population genetic model of phenotypic/genotypic clines demonstrates that there is selection against red colors in allopatry. Source of selection remains unknown. High Flower color variation is completely explained by regulatory changes in two genes (flavanone-3′5′-hydroxylase, R2R3-Myb) controlling the type and amount of anthocyanin in flowers Hopkins and Rausher (2011 , 2014 ), Hopkins et al. (2014) 
Timema cristinae Female mate choice Sexual selection favoring local male types. Females discriminate against “foreign” males High Unknown  Nosil et al . (2003 , 2012 )  
Species Trait Selection Gene flow? Genetic basis References 
Drosophila serrata Male cuticular hydrocarbons (CHCs) have diverged between sympatric and allopatric populations. Female preference is based on CHCs and has also diverged. Divergent natural between sympatry and allopatry. Sexual selection opposes reinforcing selection Unknown Differences in cuticular hydrocarbon profiles are explained by a few loci of large effect; one known locus: mFAS (12–30% of PV) Higgie et al. (2000) ; Higgie and Blows (2008) ; Hine et al. (2011) ; Chung et al. (2014) 
Drosophila mojavensis Female preferences differ between sympatric and allopatric populations. Male CHCs are hypothesized to have diverged as well. Unknown  Moderate to high among populations of D. mojavensis. Early in the divergence between D. arizonae and D. mojavensis Hypothesized to be mono- or oligogenic. Male and female courtship behaviors might be under the control of separate alleles or sex-specific behaviors are controlled by the same gene or genes acting in a sex-specific manner. The specific details remain unknown Wasserman and Koepfer (1977) ; Zouros and D’Entremont (1980) ; Markow (1991) ; Massie and Markow (2005) ; Ross and Markow (2006) ; Lohse et al . (2015) ,Jennings and Etges 2010 
Drosophila subquinaria Both male and female CHCs differ between sympatric and allopatric populations. Clines in mate discrimination and genetic markers suggest reinforcing selection is advantageous only in sympatry Reduced gene flow inferred from clines, but not directly measured. Unknown  Jaenike et al . (2006) ; Curtis et al . (2013) ; Giglio and Dyer (2013) ; Bewick and Dyer (2014) ; Dyer et al . (2014)  
Drosophila yakuba Gametic incompatibility between sympatric and allopatric populations. Female traits involved in retention or use of sperm. Clines in gametic isolation suggest reinforcing selection is advantageous only in sympatry. Mitochondrial introgression in the São Tomé hybrid zone. Moderate evidence of nuclear introgression between species and extensive gene flow between allopatric and sympatric lines Unknown Llopart et al. (2005) ; Bachtrog et al. (2008) ; Beck et al. (2015) 
Litoria verreauxii Male call differs between sympatric and allopatric populations. Unknown Unknown Unknown Littlejohn and Loftus-Hills (1968) 
Lucania parva Unknown, but potentially linked to body length and size of anal fin Unknown Unknown Unknown Kozak et al. (2015) 
Pseudacris feriarum Male call and female preference differ among multiple hybrid zones Not measured, but aspects of mating signal favored in sympatry might be costly in allopatry. Possible case of convergent reinforcing selection Unknown Unknown Lemmon (2009) 
Litoria genimaculata Male call differs among populations. Individuals from contact zones are discriminated upon by allopatric individuals Unknown Unknown Hoskin et al. (2005) 
Spea multiplicata  Male call and female choice have evolved via reinforcement in areas where S. bombifrons is present  Unknown  Gene flow is slightly reduced among sympatric and allopatric populations. No information of gene flow between S. multiplicata and S. bombifrons Unknown Pfennig and Simovich (2002) ; Pfennig and Pfennig (2005) ; Pfennig and Rice (2014) 
Gryllus fultoni Calling song/female preference Not measured yet, but females prefer local song types. Possible case of a one-allele mechanism Unknown Unknown Jang and Gerhardt (2006a , b )  
Magicicada neotredecim Calling song/female preference Not measured, but females prefer local song types. Possible case of a one-allele discrimination model Unknown Unknown  Cooley et al . (2006)  
Phlox drumondii  Flower color and hue have evolved under reinforcing selection in areas where P. cuspidata is also present. Reproductive isolation between red and blue morphs of P. drumondii driven by selection against migrants . Population genetic model of phenotypic/genotypic clines demonstrates that there is selection against red colors in allopatry. Source of selection remains unknown. High Flower color variation is completely explained by regulatory changes in two genes (flavanone-3′5′-hydroxylase, R2R3-Myb) controlling the type and amount of anthocyanin in flowers Hopkins and Rausher (2011 , 2014 ), Hopkins et al. (2014) 
Timema cristinae Female mate choice Sexual selection favoring local male types. Females discriminate against “foreign” males High Unknown  Nosil et al . (2003 , 2012 )  

For each system we give the species, the putative trait subject to reinforcing selection, whether selection has been measured for that trait between conspecific populations occurring in sympatry and allopatry (with respect to a second species driving reinforcement), if gene flow has been estimated between populations found in sympatry and allopatry (Gene flow?), and whether the genetic basis of those traits is known. This table was inspired by, and shows some overlap with table 3 of Ortiz-Barrientos et al. (2009); however, we have included additional cases (e.g., D. mojavensis , P. drummondii , and D. yakuba ). References for each of the systems are given in the final column.

A (Verbal) Population Genetics Model of CER

Factors predicted to affect the likelihood of CER

The examples presented above and in Table 1 suggest that CER are feasible. However, there is currently little formal quantitative/population genetic theory available to predict when CER should occur (but see Yukilevich and Aoki, this column). Below, we discuss how pre-existing theory developed to understand the parameters affecting local adaptation and reinforcement may be applicable to CER.

As discussed above, reinforcement can lead to local adaptation in prezygotic traits, resulting in differentiation among conspecific populations. In general, differentiation between populations subject to divergent selection (as when s–a effects are observed) represents a balance of multiple factors including selection favoring the local adaptation (s 1 ), selection against the adaptation outside of regions where it is advantageous (s 2 ), gene flow among populations ( m ; realized migration), and the effective population size (Ne) ( Slatkin 1975 , 1987 ; Barton and Bengtsson 1986 ; Yeaman and Otto 2011 ). However, RRI differs from other adaptations in the sense that there are two levels of gene flow ( m ) that are important for the evolution of the trait: gene flow between the hybridizing species (m 1 ), and gene flow between allopatric and sympatric populations of the same species (m 2 ). The role of selection and m 1 in reinforcement has been dealt with extensively elsewhere ( Liou and Price 1994 ; Kelly and Noor 1996 ; Servedio and Kirkpatrick 1997 ; Servedio and Noor 2003 ). In general, these studies show that reinforcement is more likely to lead to speciation when hybrid offspring have very low fitness and when there is a mechanism causing linkage disequilibrium (LD) between the alleles underlying hybrid dysfunction and those controlling prezygotic isolation ( Servedio 2009 ).

Explicit treatments of the factors affecting CER remain much less common than those affecting reinforcement (however, see Pfennig and Ryan 2006 ; McPeek and Gavrilets 2006 ). On the other hand, the general roles of selection and gene flow in facilitating adaptive differentiation between populations have received much more attention. Theoretical studies of local adaptation and hybrid zones are particularly germane to CER because they provide a framework for understanding the geographical distribution of an allele that is locally adaptive in a particular location, but neutral or deleterious elsewhere (e.g., Haldane 1948 ; Barton and Bengtsson 1986 ; Slatkin 1987 ). Additional work has addressed the role of genetics in facilitating (or constraining) differentiation in the face of gene flow ( Yeaman and Otto 2011 ; Yeaman and Whitlock 2011 ; Bank et al . 2012 ; Yeaman 2015 ). These bodies of theory could be used to help predict the conditions most conducive to CER because they deal with the roles of selection and gene flow in promoting and maintaining differentiation between populations (see reviews by Kawecki and Ebert 2004 ; Nosil et al . 2009 ; Savolainen et al . 2013 ).

Two factors—selection and migration—have arguably received the most theoretical attention with respect to their role in the evolution of phenotypic differentiation and reproductive isolation between populations, especially in the context of clines and hybrid zones ( Slatkin 1975 , 1987 ; Barton and Bengtsson 1986 ; Hendry et al . 2002 ; Moore et al . 2007 ; Bank et al . 2011 , 2012 ). These studies describe how differentiation can be maintained among conspecific populations when the strength of selection acting among populations is greater than rates of gene flow ( Haldane 1948 ; Barton 1979 ; Szymura and Barton 1986 ; Jiggins and Mallet 2000 ). In neutral cases, we expect population differentiation if m is much smaller than 1/4Ne (for diploid populations; Slatkin and Maruyama 1975 ). Generally speaking, these results mean that s 1 , s 2 , and m 2 will all influence the likelihood of CER and highlight the importance of understanding their magnitude in natural populations.

A third factor—the genetic basis of traits—has received significant attention in the reinforcement literature ( Liou and Price 1994 ; Servedio and Noor 2003 ). With respect to reinforcement, a genetic mechanism linking the traits generating prezygotic isolation and those causing hybrid dysfunction can help to facilitate the evolution of strong prezygotic isolation and speciation (see Servedio and Noor 2003 and references therein for details). Both the physical clustering of loci in the genome and assortative mating driven by the action of a single allele have been discussed as mechanisms that can facilitate this LD. The former mechanism can promote speciation by reinforcement because it reduces recombination between loci involved in prezygotic and postzygotic isolation ( Felsenstein 1981 ; Liou and Price 1994 ). The latter mechanism (frequently referred to as the “one-allele” model) can promote reinforcement because reproductive isolation is the result of a single allele that causes assortative mating irrespective of the genetic background it is found in (e.g., an allele causing individuals to mate with individuals more phenotypically similar to themselves or to reject heterospecifics in general). Since recombination cannot affect reproductive isolation caused by a one-allele mechanism, this mechanism has been considered particularly powerful for speciation by reinforcement ( Ortiz-Barrientos et al . 2004 ; Ortíz-Barrientos and Noor 2005 ; Bank et al . 2012 ).

Unlike reinforcement, the genetics of CER does not require LD between the alleles generating hybrid dysfunction and those underlying prezygotic isolation. Therefore, it is unknown whether genetic mechanisms favoring reinforcement, such as the one-allele mechanism, are likely to lead to CER. For example, if reinforcement causes sympatric populations to differentiate from allopatric populations with respect to a trait crucial for the recognition of conspecific mates, then strong-LD or one-allele mechanisms could promote CER. By contrast, a “discrimination” allele that strengthens one’s ability to actively locate and secure conspecific mates could be favored in all populations and rapidly spread throughout a species’ range. This second scenario would not constitute a CER because there would be no reproductive isolation among conspecific populations. Dissecting the genetic basis of the traits involved in reinforcement and CER provides an exciting opportunity to clarify the genetic mechanisms most likely to lead to CER and connect microevolutionary processes such as selection on particular alleles with macroevolutionary processes such as speciation.

Factors affecting c-s effects

C-s effects rely on the convergent evolution of populations experiencing parallel reinforcing selection. This is because different phenotypic and genetic solutions are required to facilitate the differentiation of conspecific traits, and different genetic variants fixed in different populations will potentially be incompatible and generate RI when brought together. Theoretical work explicitly testing the demographic and genetic factors affecting the likelihood of c-s effects are needed, however others have discussed how the genetic basis of parallel phenotypic adaptation will depend on genetic, mutational, and demographic factors ( Stern and Orgogozo 2008 , 2009 ; Ralph and Coop 2015 ). For example, recent theoretical work has shown how parallel adaptation can frequently occur through different genetic mechanisms when population sizes are large, there are many mutational targets underlying adaptive phenotypic variation ( Ralph and Coop 2015 ), and rates of gene flow between the populations adapting in parallel are low ( Nosil and Flaxman 2011 ; Ralph and Coop 2015 ). In some ways these results suggest that the “simple” genetic control predicted for reinforced traits may result in c-s effects being less likely. For example, a trait under simple genetic control will have fewer mutation targets than a highly polygenic trait. However, this depends on the dimensionality of phenotypic adaptation, and large mutational targets can be manifest through either polygenic control of as single trait, or simple, and independent, control of many traits ( Nosil and Hohenlohe 2012 ). These predictions and scenarios highlight how identifying the traits and genes that are targets of reinforcement will help us to better understand and predict reinforcement’s evolutionary consequences, especially with respect to genetic differentiation among conspecific populations.

Factors affecting s–a effects

S–a effects require the alleles underlying reinforced phenotypes to be under divergent selection between sympatric and allopatric regions of a species’s range (i.e., traits are favored in sympatry but disadvantageous in allopatry, a type of Genotype × Environment interaction). There are three parameters that are therefore expected to influence the magnitude of s–a effects: s 1 , s 2 , and m 2 ( Haldane 1948 ; Barton 1983 ) . When reinforced phenotypes are advantageous in sympatry but deleterious in allopatry ( s1  > 0 and s2  < 0), their underlying alleles are expected to be structured geographically depending on the relative magnitudes of s 1 , s 2 , and the rate of migration between populations [m 2 ; a full theoretical treatment on the subject can be found in Bank et al . (2012) ]. Direct measurements of selection acting on the phenotypes involved in reinforcement in sympatric and allopatric regions of the same species’ range (i.e., s 1 and s 2 ) remain rare (however, see: Bewick and Dyer 2014 ; Hopkins and Rausher 2014 ; Hopkins et al . 2014 ). Studies of the Texas wildflower P.drummondii arguably provide the best example of how characterizing selection, gene flow, and the genetic basis of reinforced phenotypes can help explain their observed geographic distributions and evolutionary relevance ( Hopkins and Rausher 2014 ; Hopkins et al . 2014 ). Estimating these parameters in other systems undergoing reinforcement are required to verify whether observed clines in reinforced phenotypes (i.e., a pattern of RCD) are simply due to geographical isolation present between conspecific populations or reflect true CER.

Future Directions and Conclusion

Our understanding of CER could be strengthened through the development of three avenues of research. First, we need to establish how frequently reinforcement has cascading effects among populations of the same species and quantify the magnitude of those effects. A considerable proportion of the systems where reinforcement is acting have also shown evidence of CER (see Table 1 for examples). However, for many of these cases we do not know the magnitude of RI that exists between allopatric and sympatric populations of conspecifics, or the specific phenotypes involved in generating RI, making it difficult to establish the importance of reinforcement in incidentally promoting differentiation and ultimately speciation among conspecifics.

A second avenue of research is the development of alternative approaches for detecting CER. All cases in which CER have been detected rely on the observation of RCD in sympatry and differentiation between conspecific populations. Nonetheless, we know that reinforcement does not always generate RCD (i.e., stronger reproductive isolation spreads from the hybrid zone throughout the whole range of a species; Noor 1997 ) and that not all RCD is caused by reinforcement ( Brown and Wilson 1956 ; Walker 1974 ). A simple, but not always feasible, approach to detecting CER is the use of time-series data collected to measure how the magnitude of reproductive isolation and levels of hybridization change through time ( Pfennig 2003 ). This, of course, will only be possible for organisms with relatively short generation times, rapid evolutionary responses to reinforcing selection ( Pfennig 2003 ), and/or those that are amenable to experimental evolution in the lab (e.g., Drosophilid flies, Matute 2010 ; Comeault et al . 2015b ; Neurospora, Turner et al . 2010 ; Saccharomyces , Murphy and Zeyl 2015 ).

The development of phylogenetic comparative or population genetic methods for detecting CER would be a more generalizable approach. Reinforcement can leave a signature on phylogenies. Noor (1997) proposed a simple yet powerful test to compare the magnitude of reproductive isolation in a phylogenetic framework. The premise of this approach is to use three closely related species (2 sister species “A” and “B”, and an outgroup “C”). The triad must fulfill the following criteria: one of the sister species (A) must be sympatric with the outgroup (C), and the other (B) must be allopatric to both species (A and C). If reinforcement has played a role in the evolution of reproductive isolation in the sympatric species (A), then it should show greater species discrimination toward (C) than the allopatric species (B). Noor (1997) used this approach and found that reinforcement has played a role in 21% of the Drosophila species examined. This type of approach does not exist for detecting CER and its development could be critical for organisms in which measuring reproductive isolation in the laboratory is not feasible. While controlling for the divergence time between sister species, the expectation of a phylogenetic approach for detecting CER would be that if CER were common, levels of differentiation among conspecific populations (measured as genetic or phenotypic differentiation) should be greater in those systems where reinforcement occurs when compared with those systems where it does not. The challenge to this type of approach will be in determining the systems (and populations) where reinforcement is or is not occurring. However, patterns such as asymmetries in the cost of hybrid matings can be used to define species that are more likely to be affected by reinforcement ( Yukilevich 2012 ). This information could then be used to predict the species that are most likely to show CER.

A third avenue of research that would benefit the study of CER would be to determine the genetics of the traits involved in reinforcement. The genetics of RRI remains largely unknown, and even less is known regarding whether the traits that respond to reinforcing selection are the same as those that lead to CER. Disentangling whether RRI toward heterospecifics shares the same genetic basis as its cascading effects is crucial to understanding the mechanism leading to both reproductive isolation between heterospecifics and that observed between conspecifics. For example, this would allow us to determine whether CER are a consequence of direct selection or selection through linkage (i.e., hitchhiking).

CER represent a mechanism through which reinforcement can not only complete speciation after secondary contact, but can also promote additional speciation events between conspecific populations. Current evidence indicates that CER can lead to the origin of moderate levels of reproductive isolation (see examples in Table 1 ). Speciation, however, involves the origin of new barriers and the persistence of reproductively isolated lineages. It remains to be shown whether the CER can indeed drive the diversification of lineages that persist over time or whether they are transient patterns observed during the completion of speciation by reinforcement.

Glossary of Terms

Reinforcement: the process where selection against maladapted hybrid offspring indirectly selects for, and causes the evolution of, increased prezygotic isolation between two co-occurring species.

RCD: a pattern generated when competition between two species causes phenotypes to shift in one or both interacting species such that competition is minimized. RCD is commonly (but not always) generated by reinforcement and is frequently identified by comparing the distribution of phenotypes observed in populations of a species that co-occur with a competing species with those of conspecific populations that are found in allopatry. In reproductive character displacement, the phenotypes that are displaced in sympatry affect phenotypes used in mate recognition, mate choice, or fertility.

CER: incidental effects that reinforcement can have on levels of reproductive isolation between populations of the same species.

RRI: isolation between two species that evolves as a result of reinforcing selection.

C-s effects: CER that are the result of convergent responses to reinforcing selection acting in parallel in multiple populations of the same (focal) species.

S–a effects: CER that are the result of alleles or phenotypes that are favored by reinforcing selection in the sympatric (with respect to a second species) part of a species’ range, but selected against in allopatric regions of that same species’ range.

Acknowledgments

We are grateful to D. A. Turissini, members of the Matute lab, and three anonymous reviewers for helpful comments and feedback on previous versions of this manuscript. We also thank Becky Fuller for inviting us to contribute to this section and providing extensive, and constructive, comments that greatly improved this manuscript.

References

Abbott
R
Albach
D
Ansell
S
Arntzen
JW
Baird
SJE
et al
.,
2013
.
Hybridization and speciation
.
J Evol Biol
 
26
:
229
246
.
Bachtrog
D
Thornton
K
Clark
A
Andolfatto
P
,
2006
.
Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group
.
Evolution
 
60
:
292
302
.
Bank
C
Bürger
R
Hermisson
J
,
2012
.
The limits to parapatric speciation: Dobzhansky-Muller incompatibilities in a continent-Island model
.
Genetics
 
191
:
845
863
.
Bank
C
Hermisson
J
Kirkpatrick
M
,
2011
.
Can reinforcement complete speciation?
Evolution
 
66
:
229
239
.
Barton
NH
,
1979
.
The dynamics of hybrid zones
.
Heredity
 
43
:
341
359
.
Barton
NH
,
1983
.
Multilocus clines
.
Evolution
 
37
:
454
471
.
Barton
N
Bengtsson
BO
,
1986
.
The barrier to genetic exchange between hybridising populations
.
Heredity
 
56
:
357
376
.
Beck
EA
Thompson
AC
Sharbrough
J
Brud
E
Llopart
A
,
2015
.
Gene flow between Drosophila yakuba and Drosophila santomea in subunit V of cytochrome c oxidase: a potential case of cytonuclear cointrogression
.
Evolution
 
69
:
1973
1986
.
Bewick
ER
Dyer
KA
,
2014
.
Reinforcement shapes clines in female mate discrimination in Drosophila subquinaria
.
Evolution
 
68
:
3082
3094
.
Bolnick
DI
Near
TJ
,
2005
.
Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae)
.
Evolution
 
59
:
1754
1767
.
Brown
WL
Wilson
EO
,
1956
.
Character displacement
.
Syst Zool
 
5
:
49
64
.
Butlin
R
,
1987
.
Speciation by reinforcement
.
Trends Ecol Evol
 
2
:
8
13
.
Chung
H
Loehlin
DW
Dufour
HD
Vaccarro
K
Millar
JG
et al
.,
2014
.
A single gene affects both ecological divergence and mate choice in Drosophila
.
Science
 
343
:
1148
1151
.
Comeault
AA
Venkat
A
Matute
DR
,
2015
.
Coevolution of male and female reproductive traits drive cascading reinforcement in Drosophila yakuba . bioRxiv pre-print
.
Cooley
JR
Marshall
DC
Hill
KBR
Simon
C
,
2006
.
Reconstructing asymmetrical reproductive character displacement in a periodical cicada contact zone
.
J Evol Biol
 
19
:
855
868
.
Coyne
JA
Orr
HA
,
1989
.
Patterns of speciation in Drosophila
.
Evolution
 
43
:
362
381
.
Coyne
JA
Orr
HA
,
1997
.
Patterns of speciation in Drosophila revisited
.
Evolution
 
51
:
295
303
.
Coyne
JA
Orr
HA
,
2004
.
Speciation. Sunderland: Sinauer Associates, Inc
.
Curtis
S
Sztepanacz
JL
White
BE
Dyer
KA
Rundle
HD
et al
.,
2013
.
Epicuticular compounds of Drosophila subquinaria and D. recens : identification, quantification, and their role in female mate choice
.
J Chem Ecol
 
39
:
579
590
.
Darwin
C
,
1859
.
On the Origin of the Species
  .
London
:
John Murray
.
Dobzhansky
T
,
1937
.
Genetics and the Origin of Species
  .
New York
:
Columbia University Press
.
Dobzhansky
T
,
1940
.
Speciation as a stage in evolutonary divergence
.
Am Nat
 
74
:
312
321
.
Dyer
KA
White
BE
Sztepanacz
JL
Bewick
ER
Rundle
HD
,
2014
.
Reproductive character displacement of epicuticular compounds and their contribution to mate choice in Drosophila subquinaria and Drosophila recens
.
Evolution
 
68
:
1163
1175
.
Felsenstein
J
,
1981
.
Skepticism towards Santa Rosalia, or why are there so few kinds of animals?
Evolution
 
35
:
124
138
.
Giglio
EM
Dyer
KA
,
2013
.
Divergence of premating behaviors in the closely related species Drosophila subquinaria and D . recens
.
Ecol Evol
 
3
:
365
374
.
Haldane
JBS
,
1948
.
The theory of a cline
.
J Genet
 
48
:
277
284
.
Harrison
RG
,
2012
.
The language of speciation
.
Evolution
 
66
:
3643
3657
.
Hendry
AP
Taylor
EB
McPhail
JD
,
2002
.
Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the Misty system
.
Evolution
 
56
:
1199
1216
.
Higgie
M
Blows
MW
,
2008
.
The evolution of reproductive character displacement conflicts with how sexual selection operates within a species
.
Evolution
 
62
:
1192
1203
.
Higgie
M
Chenoweth
S
Blows
MW
,
2000
.
Natural selection and the reinforcement of mate recognition
.
Science
 
290
:
519
521
.
Hine
E
McGuigan
K
Blows
MW
,
2011
.
Natural selection stops the evolution of male attractiveness
.
Proc Natl Acad Sci USA
 
108
:
3659
3664
.
Hopkins
R
Guerrero
RF
Rausher
MD
Kirkpatrick
M
,
2014
.
Strong reinforcing selection in a Texas wildflower
.
Curr Biol
 
24
:
1
5
.
Hopkins
R
Rausher
MD
,
2011
.
Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii
.
Nature
 
469
:
411
414
.
Hopkins
R
Rausher
MD
,
2012
.
Pollinator-mediated selection on flower color allele drives reinforcement
.
Science
 
335
:
1090
1092
.
Hopkins
R
Rausher
MD
,
2014
.
The cost of reinforcement: selection on flower color in allopatric populations of Phlox drummondii
.
Am Nat
 
183
:
693
710
.
Hoskin
CJ
Higgie
M
,
2010
.
Speciation via species interactions: the divergence of mating traits within species
.
Ecol Lett
 
13
:
409
420
.
Hoskin
CJ
Higgie
M
McDonald
KR
Moritz
C
,
2005
.
Reinforcement drives rapid allopatric speciation
.
Nature
 
437
:
1353
1356
.
Howard
DJ
,
1993
.
Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis
. In:
Harrison
RG
, editor.
Hybrid Zones and the Evolutionary Process
  .
Oxford
:
Oxford University Press
,
46
69
.
Hudson
EJ
Price
TD
,
2014
.
Pervasive reinforcement and the role of sexual selection in biological speciation
.
J Hered
 
105
:
821
833
.
Jaenike
J
Dyer
KA
Cornish
C
Minhas
MS
,
2006
.
Asymmetrical reinforcement and Wolbachia infection in Drosophila
.
PLoS Biol
 
4
:
1852
1862
.
Jang
Y
Gerhardt
HC
,
2006a
.
Divergence in the calling song between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni (Orthoptera: Gryllidae)
.
J Evol Biol
 
19
:
459
472
.
Jang
Y
Gerhardt
HC
,
2006b
.
Divergence in female calling song discrimination between sympatric and allopatric populations of the southern wood cricket Gryllus fultoni , (Orthoptera: Gryllidae)
.
Behav Ecol Sociobiol
 
150
:
150
158
.
Jennings
JH
Etges
WJ
,
2010
.
Species hybrids in the laboratory but not in nature: a reanalysis of premating isolation between Drosophila arizonae and D. mojavensis
.
Evolution
 
64
(
2
):
587
598
.
Jiggins
C
Mallet
J
,
2000
.
Bimodal hybrid zones and speciation
.
Trends Ecol Evol
 
15
:
250
255
.
Kawecki
TJ
Ebert
D
,
2004
.
Conceptual issues in local adaptation
.
Ecol Lett
 
7
:
1225
1241
.
Kay
KM
Schemske
DW
,
2008
.
Natural selection reinforces speciation in a radiation of neotropical rainforest plants
.
Evolution
 
62
:
2628
2642
.
Kelly
JK
Noor
M AF
,
1996
.
Speciation by reinforcement: a model derived from studies of Drosophila
.
Genetics
 
143
:
1485
1497
.
Koopman
KKF
,
1950
.
Natural selection for reproductive isolation between Drosophila pseudoobscura and Drosophila persimilis
.
Evolution
 
4
:
135
148
.
Kozak
GM
Roland
G
Rankhorn
C
Falater
A
Berdan
EL
et al
.,
2015
.
Behavioral isolation due to cascade reinforcement in Lucania killifish
.
Am Nat
 
185
:
491
506
.
Lemmon
AR
Smadja
C
Kirkpatrick
M
,
2004
.
Reproductive character displacement is not the only possible outcome of reinforcement
.
J Evol Biol
 
17
:
177
183
.
Lemmon
EM
,
2009
.
Diversification of conspecific signals in sympatry: geographic overlap drives multidimensional reproductive character displacement in frogs
.
Evolution
 
63
:
1155
1170
.
Liou
LW
Price
TD
,
1994
.
Speciation by reinforcement of premating isolation
.
Evolution
 
48
:
1451
1459
.
Littlejohn
MJ
Loftus-Hills
JJ
,
1968
.
An experimental evaluation of premating isolation in the Hyla ewingi Complex (Anura:Hylidae)
.
Evolution
 
22
:
659
663
.
Llopart
A
Lachaise
D
Coyne
JA
.
2005
.
Multilocus analysis of introgression between two sympatric sister species of Drosophila : Drosophila yakuba and D
.
santomea. Genetics
 
171
:
197
210
.
Lohse
K
Clarke
M
Ritchie
MG
Etges
WJ
,
2015
.
Genome-wide tests for introgression between cactophilic Drosophila implicate a role of inversions during speciation
.
Evolution
 
69
:
1178
1190
.
Lorch
PD
Servedio
MR
,
2007
.
The evolution of conspecific gamete precedence and its effect on reinforcement
.
J Evol Biol
 
20
:
937
949
.
Maan
ME
Seehausen
O
,
2011
.
Ecology, sexual selection and speciation
.
Ecol Lett
 
14
:
591
602
.
Mani
GS
Clarke
BC
,
1990
.
Mutational order: a major stochastic process in evolution
.
Proc R Soc B: Biol Sci
 
240
:
29
37
.
Markow
TA
,
1991
.
Sexual isolation among populations of Drosophila mojavensis
.
Evolution
 
45
:
1525
1529
.
Massie
KR
Markow
TA
,
2005
.
Sympatry, allopatry and sexual isolation between Drosophila mojavensis and D
.
arizonae . Hereditas
 
142
:
51
55
.
Matute
DR
,
2010
.
Reinforcement can overcome gene flow during speciation in Drosophila
.
Curr Biol
 
20
:
2229
2233
.
Matute
DR
Butler
IA
Turissini
DA
Coyne
JA
,
2010
.
A test of the snowball theory for the rate of evolution of hybrid incompatibilities
.
Science
 
329
:
1518
1521
.
McPeek
MA
Gavrilets
S
,
2006
.
The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation
.
Evolution
 
60
:
1967
1980
.
Moore
J-S
Gow
JL
Taylor
EB
Hendry
AP
,
2007
.
Quantifying the constraining influence of gene flow on adaptive divergence in the lake-stream threespine stickleback system
.
Evolution
 
61
:
2015
2026
.
Moyle
LC
Nakazato
T
,
2010
.
Hybrid incompatibility “snowballs” between Solanum species
.
Science
 
329
:
1521
1523
.
Murphy
HA
Zeyl
CW
,
2015
.
A potential case of reinforcement in a facultatively sexual unicellular eukaryote
.
Am Nat
 
186
:
312
319
.
Noor
MA
,
1995
.
Speciation driven by natural selection in Drosophila
.
Nature
 
375
:
674
675
.
Noor
MAF
,
1997
.
How often does sympatry affect sexual isolation in Drosophila ?
Am Nat
 
149
:
1156
1163
.
Noor
MAF
,
1999
.
Reinforcement and other consequences of sympatry
.
Heredity
 
83
:
503
508
.
Nosil
P
,
2012
.
Ecological Speciation
  .
New York
:
Oxford University Press
.
Nosil
P
Crespi
BJ
Sandoval
CP
,
2003
.
Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement
.
Proc R Soc B: Biol Sci
 
270
:
1911
1918
.
Nosil
P
Flaxman
SM
,
2011
.
Conditions for mutation-order speciation
.
Proc R Soc B: Biol Sci
 
278
:
399
407
.
Nosil
P
Funk
DJ
Ortiz-Barrientos
D
,
2009
.
Divergent selection and heterogeneous genomic divergence
.
Mol Ecol
 
18
:
375
402
.
Nosil
P
Gompert
Z
Farkas
TE
Comeault
AA
Feder
JL
et al
.,
2012
.
Genomic consequences of multiple speciation processes in a stick insect
.
Proc R Soc B: Biol Sci
 
279
:
5058
5065
.
Nosil
P
Hohenlohe
PA
,
2012
.
Dimensionality of sexual isolation during reinforcement and ecological speciation in Timema cristinae stick insects
.
Evol Ecol Res
 
14
:
467
485
.
Ortiz-Barrientos
D
Counterman
BA
Noor
MAF
,
2004
.
The genetics of speciation by reinforcement
.
PLoS Biol
 
2
:
e416
.
Ortiz-Barrientos
D
Grealy
A
Nosil
P
,
2009
.
The genetics and ecology of reinforcement: implications for the evolution of prezygotic isolation in sympatry and beyond
.
Ann NY Acad Sci
 
1168
:
156
182
.
Ortíz-Barrientos
AD
Noor
MAF
,
2005
.
Evidence for a one-allele assortative mating locus
.
Science
 
310
:
1467
.
Pfennig
KS
,
2003
.
A test of alternative hypotheses for the evolution of reproductive isolation between spadefoot toads: support for the reinforcement hypothesis
.
Evolution
 
57
:
2842
2851
.
Pfennig
KS
Pfennig
DW
,
2005
.
Character displacement as the “best of a bad situation”: fitness trade-offs resulting from selection to minimize resource and mate competition
.
Evolution
 
59
:
2200
2208
.
Pfennig
KS
Rice
AM
,
2014
.
Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads
.
Proc R Soc B: Biol Sci
 
281
:
20140949
.
Pfennig
KS
Ryan
MJ
,
2006
.
Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study
.
Proc R Soc B: Biol Sci
 
273
:
1361
1368
.
Pfennig
KS
Simovich
MA
,
2002
.
Differential selection to avoid hybridization in two toad species
.
Evolution
 
56
:
1840
1848
.
Rabosky
DL
Matute
DR
,
2013
.
Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds
.
Proc Natl Acad Sci USA
 
110
:
15354
15359
.
Ralph
PL
Coop
G
,
2015
.
The role of standing variation in geographic convergent adaptation
.
Am Nat
 
186
:
S000
S000
.
Ross
CL
Markow
TA
,
2006
.
Microsatellite variation among diverging populations of Drosophila mojavensis
.
J Evol Biol
 
19
:
1691
1700
.
Rundle
HD
Nosil
P
,
2005
.
Ecological speciation
.
Ecol Lett
 
8
:
336
352
.
Sanderson
N
,
1989
.
Can gene flow prevent reinforcement?
Evolution
 
43
:
1223
1235
.
Savolainen
O
Lascoux
M
Merilä
J
,
2013
.
Ecological genomics of local adaptation
.
Nat Rev Genet
 
14
:
807
820
.
Schluter
D
,
2009
.
Evidence for ecological speciation and its alternative
.
Science
 
323
:
737
741
.
Seehausen
O
Terai
Y
Magalhaes
IS
Carleton
KL
Mrosso
HDJ
et al
.,
2008
.
Speciation through sensory drive in cichlid fish
.
Nature
 
455
:
620
626
.
Servedio
M
Kirkpatrick
M
,
1997
.
The effects of gene flow on reinforcement
.
Evolution
 
51
:
1764
1772
.
Servedio
MR
,
2009
.
The role of linkage disequilibrium in the evolution of premating isolation
.
Heredity
 
102
:
51
56
.
Servedio
MR
Noor
M
,
2003
.
The role of reinforment in speciation: theory and data
.
Annu Rev Ecol Evol Syst
 
34
:
339
364
.
Slatkin
M
,
1975
.
Gene flow and selection in a two-locus system
.
Genetics
 
81
:
787
802
.
Slatkin
M
,
1987
.
Gene flow and the geographic structure of natural populations
.
Science
 
236
:
787
792
.
Slatkin
M
Maruyama
T
,
1975
.
Genetic drift in a cline
.
Genetics
 
81
:
209
222
.
Spencer
Hamish
G
McArdle
BH
Lambert
DM
,
1986
.
A theoretical investigation of speciation by reinforcement
.
Am Nat
 
128
:
241
262
.
Stern
DL
Orgogozo
V
,
2008
.
The loci of evolution: how predictable is genetic evolution?
Evolution
 
62
:
2155
2177
.
Stern
DL
Orgogozo
V
,
2009
.
Is genetic evolution predictable?
Science
 
323
:
746
751
.
Szymura
JM
Barton
NH
,
1986
.
Genetic analysis of a hybrid zone between the fire-bellied toads Bombina bombina and B. variegata , near Cracow in southern Poland
.
Evolution
 
40
:
1141
1159
.
Templeton
AR
,
1981
.
Mechanisms of speciation: a population genetic approach
.
Ann Rev Ecol Syst
 
12
:
23
48
.
Turner
E
Jacobson
DJ
Taylor
JW
,
2010
.
Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus
.
J Evol Biol
 
23
:
1642
1656
.
Walker
TJ
,
1974
.
Character displacement and acoustic insects
.
Am Zool
 
14
:
1137
1150
.
Wasserman
M
Koepfer
HR
,
1977
.
Character displacement for sexual isolation between Drosophila majavensis and Drosophila arizonensis
.
Evolution
 
31
:
812
823
.
Yeaman
S
,
2015
.
Local adaptation by alleles of small effect
.
Am Nat
 
186
:
S74
S89
.
Yeaman
S
Otto
SP
,
2011
.
Establishment and maintenance of adaptive genetic divergence under migration, selection, and drift
.
Evolution
 
65
:
2123
2139
.
Yeaman
S
Whitlock
MC
,
2011
.
The genetic architecture of adaptation under migration-selection balance
.
Evolution
 
65
:
1897
1911
.
Yukilevich
R
,
2012
.
Asymmetrical patterns of speciation uniquely support reinforcement in Drosophila
.
Evolution
 
66
:
1430
1446
.
Zouros
E
D’Entremont
CJ
,
1980
.
Sexual isolation among populations of Drosophila mojavensis : response to pressure from a related species
.
Evolution
 
34
:
421
430
.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/ ), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com