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.
Highlights
Understanding how reproductive isolation evolves is key to our understanding of speciation (Mayr 1963; Coyne and Orr 2004; our use of terms is defined in table A1)
A single locus or trait may contribute to the barrier independently
Understanding how linkage disequilibrium (LD) builds up remains an important part of research on coupling, especially since many scenarios of speciation will include two-allele mechanisms and at least some episodes of gene flow (Smadja and Butlin 2011), but this should be included in a larger set of coupling processes that build strong overall barriers to gene exchange by making multiple barrier effects coincide
Summary
Understanding how reproductive isolation evolves is key to our understanding of speciation (Mayr 1963; Coyne and Orr 2004; our use of terms is defined in table A1). Understanding how LD builds up remains an important part of research on coupling, especially since many scenarios of speciation will include two-allele mechanisms and at least some episodes of gene flow (Smadja and Butlin 2011), but this should be included in a larger set of coupling processes that build strong overall barriers to gene exchange by making multiple barrier effects coincide These considerations lead us to propose a definition of “coupling” that is general while being compatible with the different uses of the term in the existing literature and with other terminology (see table A1): coupling is any process that generates coincidence of barrier effects, resulting in a stronger overall barrier to gene flow. “Coincident,” in this context, is not restricted to have a spatial meaning: it can be in any dimension, such as in time or in some niche dimension
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