Coupling, Reinforcement, and Speciation

Abstract

During the process of speciation, populations may diverge for traits and at their underlying loci that contribute barriers to gene flow. These barrier traits and barrier loci underlie individual barrier effects, by which we mean the contribution that a barrier locus or trait-or some combination of barrier loci or traits-makes to overall isolation. The evolution of strong reproductive isolation typically requires the origin of multiple barrier effects. Critically, it also requires the coincidence of barrier effects; for example, two barrier effects, one due to assortative mating and the other due to hybrid inviability, create a stronger overall barrier to gene flow if they coincide than if they distinguish independent pairs of populations. Here, we define "coupling" as any process that generates coincidence of barrier effects, resulting in a stronger overall barrier to gene flow. We argue that speciation research, both empirical and theoretical, needs to consider both the origin of barrier effects and the ways in which they are coupled. Coincidence of barrier effects can occur either as a by-product of selection on individual barrier effects or of population processes, or as an adaptive response to indirect selection. Adaptive coupling may be accompanied by further evolution that enhances individual barrier effects. Reinforcement, classically viewed as the evolution of prezygotic barriers to gene flow in response to costs of hybridization, is an example of this type of process. However, we argue for an extended view of reinforcement that includes coupling processes involving enhancement of any type of additional barrier effect as a result of an existing barrier. This view of coupling and reinforcement may help to guide development of both theoretical and empirical research on the process of speciation.

Allopatric and sympatric diversification within roach (Rutilus rutilus) of large pre‐alpine lakes

“…For example, roach prefer warmer water and are therefore restricted to the shallow zones of lakes, whereas whitefish can tolerate colder water, allowing them to explore the deeper sections of lakes (Coutant, ; Kottelat & Freyhof, ), and (d) Recent genomic work suggests that adaptive diversification in stickleback and whitefish often occurs from standing genetic variation in genomic regions that show structural changes, including inversions (Jones et al., ; Marques et al., ) or chromosomal rearrangements (Dion‐Côté et al., ). Such structural genomic rearrangements may then facilitate diversification through coupling of co‐adapted alleles (Butlin & Smadja, ). Given the limited evidence for genetic differentiation in roach (Figure , Table S4), such genomic features may be lacking, which may constitute a genetic constraint that impedes diversification and the build‐up of genetic barriers to gene flow (Seehausen et al., ).…”

Multiple forms of selection shape reproductive isolation in a primate hybrid zone

“…Point estimates of β were much less variable for loci with a pattern of reduced introgression ( β > 0) than for loci with a pattern of increased introgression ( β < 0), particularly for β outliers (Figure ). These coincident β > 0 clines may be a reflection of the coupling of multiple barrier effects in the hybrid zone (Butlin & Smadja, ). Recent admixture between divergent populations causes correlations between linked loci that persist over many generations (Stephens, Briscoe, & O'Brien, ; Verardi, Lucchini, & Randi, ), so the effects of indirect selection on loci near barrier loci can be strong in hybrid zones.…”

“…Reinforcement enhances barriers to reproduction between species and can act to complete the speciation process when partially isolated species come into contact after experiencing some divergence in allopatry (Butlin & Smadja, ; Servedio, ). We tested for a signature of reinforcement by comparing locus‐specific differentiation between allopatric parental populations of A. palliata and A. pigra to the differentiation between backcrossed hybrids of each parental type (i.e., A. palliata ‐like and A. pigra ‐like backcrosses) in the hybrid zone for loci with reduced introgression.…”

“…This process, called reinforcement, has traditionally been considered to result in a strengthening of prezygotic barriers that prevent the formation of unfit hybrids (Butlin, ; Servedio & Noor, ). However, it has recently been extended to include the evolution of any additional barrier effect in sympatry, including postzygotic isolation, as a form of adaptive coupling of reproductive barriers (Butlin & Smadja, ). The frequency at which reinforcement occurs and its importance in shaping species diversity are open questions (Servedio, ; Servedio & Noor, ).…”

The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

“…In hybrid zones, strong post‐zygotic barriers are predicted to favour the evolution of increased prezygotic barriers through reinforcing selection (Butlin & Smadja, ; Dobzhansky, ; Servedio & Noor, ). Indeed, post‐zygotic barriers are severe in the Chrysochus hybrid zone—F1 hybrid offspring are typically sterile, regardless of cross (Peterson et al., 2005b), and we identified developmental problems in some F1 hybrids, which may be more severe in F1 hybrids with cobaltinus mothers.…”