The Genetic Architecture of Reproductive Isolation During Speciation-With-Gene-Flow in Lake Whitefish Species Pairs Assessed by Rad Sequencing

Gagnaire, Pierre‐Alexandre; Pavey, Scott A.; Normandeau, Éric; Bernatchez, Louis

doi:10.1111/evo.12075

Cited by 194 publications

(302 citation statements)

References 83 publications

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“…Bierne et al (2011) drew attention to coupling between existing intrinsic and extrinsic barrier effects, and although they considered primarily spatial interactions, they also argued that coupling is important in nonspatial dimensions. Recently, the term "coupling" has been used more widely in discussions of speciation processes (e.g., Abbott et al 2013; and empirical studies (e.g., Gagnaire et al 2013;Seehausen 2013;Vines et al 2016), reflecting an increasing recognition of its importance in the evolution of strong reproductive isolation and, thus, in the likelihood of speciation. However, because the term "coupling" has not been given a technical definition and clear delimitations, we are concerned that its actual meaning varies among authors and does not always encompass the diversity of mechanisms that could usefully be included.…”

Section: Historical Views Of Couplingmentioning

confidence: 99%

“…Although most people would agree with the idea that coupling refers to "the build-up of associations between several traits or loci that are involved in reproductive isolation [that] strengthens the total barrier to gene flow between diverging populations" (Seehausen et al 2014, p. 184), this description lacks precision and does not set clear boundaries to the concept. Some authors explicitly restrict coupling to a genomic context (genomic coupling; , consider it equivalent to "the evolution of linkage disequilibrium" (e.g., Gagnaire et al 2013;, or restrict it to two-allele barrier effects (e.g., Barton and de Cara 2009). Moreover, because conditions for coupling have mostly been explored theoretically in contexts where coupling is adaptive-that is, where it evolves as a response to selection in the presence of gene flow (e.g., Barton and de Cara 2009;Bierne et al 2011)-other possible modalities of coupling have largely been ignored.…”

Section: Historical Views Of Couplingmentioning

confidence: 99%

“…Since the temporal progression of speciation can only rarely be studied in real time, a promising direction is to compare populations at different stages of divergence in a system Shaw and Mullen 2014;Riesch et al 2017). This approach can help to reconstruct how genomic differentiation and coupling among barrier effects progress during speciation, assess whether the evolution of coupling and genome congealing (Barton 1983;Flaxman et al 2013 of chromosomal linkage and recombination rate variation in the evolution of coupling (e.g., Gagnaire et al 2013;Nadeau et al 2013;Burri et al 2015;Feulner et al 2015). Comparisons among examples with different overall barriers and different combinations of barrier effects, as well as comparative analyses of replicated and independent events of contact in a given system can also help this reconstruction (e.g., Nadeau et al 2014;Vijay et al 2017).…”

Section: Distinguishing Among Coupling Processesmentioning

confidence: 99%

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Coupling, Reinforcement, and Speciation

Butlin

Smadja

2018

The American Naturalist

167

231

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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.

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Section: Historical Views Of Couplingmentioning

confidence: 99%

Section: Historical Views Of Couplingmentioning

confidence: 99%

Section: Distinguishing Among Coupling Processesmentioning

confidence: 99%

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Coupling, Reinforcement, and Speciation

Butlin

Smadja

2018

The American Naturalist

167

231

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“…However, examples of LD estimates are relatively rare in the ecological speciation literature. We would expect a change of this trend now that new methods have been developed for the genetic analysis of species in the wild (Buerkle and Lexer, 2008;Payseur, 2010;Gompert et al, 2012;Malek et al, 2012), and that next-generation sequencing provides enough markers for extensive LD analyses in model and non-model organisms (Hohenlohe et al, 2012;Gagnaire et al, 2013). In a previous study, we showed that LD among loosely linked nuclear simple sequence repeats (nSSRs) could successfully detect footprints of divergent selection between two European white oaks (Goicoechea et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

et al. 2014

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We analyzed the genetic mosaic of speciation in two hybridizing Mediterranean white oaks from the Iberian Peninsula (Quercus faginea Lamb. and Quercus pyrenaica Willd.). The two species show ecological divergence in flowering phenology, leaf morphology and composition, and in their basic or acidic soil preferences. Ninety expressed sequence tag-simple sequence repeats (EST-SSRs) and eight nuclear SSRs were genotyped in 96 trees from each species. Genotyping was designed in two steps. First, we used 69 markers evenly distributed over the 12 linkage groups (LGs) of the oak linkage map to confirm the species genetic identity of the sampled genotypes, and searched for differentiation outliers. Then, we genotyped 29 additional markers from the chromosome bins containing the outliers and repeated the multilocus scans. We found one or two additional outliers within four saturated bins, thus confirming that outliers are organized into clusters. Linkage disequilibrium (LD) was extensive; even for loosely linked and for independent markers. Consequently, score tests for association between two-marker haplotypes and the 'species trait' showed a broad genomic divergence, although substantial variation across the genome and within LGs was also observed. We discuss the influence of several confounding effects on neutrality tests and review the evolutionary processes leading to extensive LD. Finally, we examine how LD analyses within regions that contain outlier clusters and quantitative trait loci can help to identify regions of divergence and/or genomic hitchhiking in the light of predictions from ecological speciation theory.

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“…Several studies have used linkage map information for addressing eco-evolutionary and related conservation biology issues at the species level or among hybridizing taxa (Lamaze et al 2012;Bourret et al 2013;Perrier et al 2013;Gagnaire et al 2013b;Limborg et al 2014;McKinney et al 2015). A second category of studies have focused on understanding the evolutionary consequences of the whole genome duplication event (salmonidspecific fourth vertebrate whole genome duplication; WGD-Ss4R) that occurred within the salmonid family $60 MYA (Crête-Lafrenière et al 2012), especially with regards to the partial rediploidization process, which is still underway and not totally understood yet (Berthelot et al 2014;Brieuc et al 2014;Kodama et al 2014;Sutherland et al 2016;Allendorf et al 2015;Lien et al 2016;Nugent et al 2017).…”

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confidence: 99%

A dense brown trout (Salmo trutta) linkage map reveals recent chromosomal rearrangements in theSalmogenus and the impact of selection on linked neutral diversity

Leitwein

Guinand

Pouzadoux

et al. 2016

Preprint

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High-density linkage maps are valuable tools for conservation and eco-evolutionary issues. In salmonids, a complex rediploidization process consecutive to an ancient whole genome duplication event makes linkage maps of prime importance for investigating the evolutionary history of chromosome rearrangements. Here, we developed a high-density consensus linkage map for the brown trout (Salmo trutta), a socioeconomically important species heavily impacted by human activities. A total of 3977 ddRAD markers were mapped and ordered in 40 linkage groups using sex-and lineage-averaged recombination distances obtained from two family crosses. Performing map comparison between S. trutta and its sister species, S. salar, revealed extensive chromosomal rearrangements. Strikingly, all of the fusion and fission events that occurred after the S. salar/S. trutta speciation happened in the Atlantic salmon branch, whereas the brown trout remained closer to the ancestral chromosome structure. Using the strongly conserved synteny within chromosome arms, we aligned the brown trout linkage map to the Atlantic salmon genome sequence to estimate the local recombination rate in S. trutta at 3721 loci. A significant positive correlation between recombination rate and within-population nucleotide diversity (p) was found, indicating that selection constrains variation at linked neutral sites in brown trout. This new high-density linkage map provides a useful genomic resource for future aquaculture, conservation, and eco-evolutionary studies in brown trout.

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The Genetic Architecture of Reproductive Isolation During Speciation-With-Gene-Flow in Lake Whitefish Species Pairs Assessed by Rad Sequencing

Cited by 194 publications

References 83 publications

Coupling, Reinforcement, and Speciation

Coupling, Reinforcement, and Speciation

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

A dense brown trout (Salmo trutta) linkage map reveals recent chromosomal rearrangements in theSalmogenus and the impact of selection on linked neutral diversity

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