Population genomics of parallel hybrid zones in the mimetic butterflies,<i>H. melpomene</i>and<i>H. erato</i>

Nadeau, Nicola J.; Ruiz, Mayté; Salazar, Patricio A.; Counterman, Brian A.; Medina, Jose Alejandro; Ortíz-Zuazaga, Humberto; Morrison, Anna; McMillan, W. Owen; Jiggins, Chris D.; Papa, Riccardo

doi:10.1101/000208

Cited by 51 publications

(83 citation statements)

References 83 publications

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“…The combination of large-effect switch loci and small-effect modifiers that we see in the genetic control of Heliconius wing patterning is consistent with this model, but the order in which they occurred is an important aspect of the two-step model, which we currently know little about. It is interesting to note that, in a recent analysis of divergence across hybrid zones between color-pattern races of H. erato and H. melpomene, Nadeau et al (2014) found strong divergence centered on large-effect mimicry loci in both species, but divergence associated with putative modifiers differed between species ( Figure 3C). This result may indicate that large-effect loci are conserved among species but modifiers are not.…”

Section: Molecular Characterization Of Mimicry Locimentioning

confidence: 87%

“…This was unexpected because H. melpomene and H. cydno are closely related, partially interfertile species, and their divergent color patterns have been shown to play an important role in mediating reproductive isolation. Giraldo et al (2008), Merot et al (2013), andNadeau et al (2014) have since revealed this to be a general phenomenon: there are populations of the H. cydno relative H. timareta mimicking H. melpomene all along the western side of the Andes mountains. Because hybridization between H. melpomene and the H. cydno/timareta clade is widespread, interspecific gene flow could be the source of their shared warning patterns.…”

Section: Genetic Basis Of Convergencementioning

confidence: 99%

“…Perhaps the most extreme example of this is the case of H. melpomene and H. erato Sheppard et al 1985;Brower 1994Brower , 1996bTurner and Mallet 1996;Flanagan et al 2004;Quek et al 2010;Hines et al 2011;Nadeau et al 2014). These two species are distributed throughout much of South and Central America, and they mimic one another wherever they co-occur.…”

Section: Müllerian Mimicrymentioning

confidence: 99%

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The Functional Basis of Wing Patterning inHeliconiusButterflies: The Molecules Behind Mimicry

2015

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Wing-pattern mimicry in butterflies has provided an important example of adaptation since Charles Darwin and Alfred Russell Wallace proposed evolution by natural selection .150 years ago. The neotropical butterfly genus Heliconius played a central role in the development of mimicry theory and has since been studied extensively in the context of ecology and population biology, behavior, and mimicry genetics. Heliconius species are notable for their diverse color patterns, and previous crossing experiments revealed that much of this variation is controlled by a small number of large-effect, Mendelian switch loci. Recent comparative analyses have shown that the same switch loci control wing-pattern diversity throughout the genus, and a number of these have now been positionally cloned. Using a combination of comparative genetic mapping, association tests, and gene expression analyses, variation in red wing patterning throughout Heliconius has been traced back to the action of the transcription factor optix. Similarly, the signaling ligand WntA has been shown to control variation in melanin patterning across Heliconius and other butterflies. Our understanding of the molecular basis of Heliconius mimicry is now providing important insights into a variety of additional evolutionary phenomena, including the origin of supergenes, the interplay between constraint and evolvability, the genetic basis of convergence, the potential for introgression to facilitate adaptation, the mechanisms of hybrid speciation in animals, and the process of ecological speciation.

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Section: Molecular Characterization Of Mimicry Locimentioning

confidence: 87%

Section: Genetic Basis Of Convergencementioning

confidence: 99%

Section: Müllerian Mimicrymentioning

confidence: 99%

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The Functional Basis of Wing Patterning inHeliconiusButterflies: The Molecules Behind Mimicry

2015

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“…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). In general, it will be important to identify more systems offering multiple hybrid zones to compare situations where coupling may not be at the same stage across the distribution range (e.g., in common voles [Beysard and Heckel 2014], Hyla frogs [Dufresnes et al 2015], or green toads [Dufresnes et al 2014]).…”

Section: Distinguishing Among Coupling Processesmentioning

confidence: 99%

Coupling, Reinforcement, and Speciation

Butlin

Smadja

2018

The American Naturalist

192

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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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“…There are a few examples of RADseq genome scans recovering loci previously known to be involved in adaptive divergence (Hohenlohe et al 2010;Nadeau et al 2014). Further, some methylation-sensitive restriction enzymes do preferentially target genic regions of the genome (Pegadaraju et al 2013).…”

Section: If You Radmentioning

confidence: 99%

Breaking RAD: An evaluation of the utility of restriction site associated DNA sequencing for genome scans of adaptation

et al. 2016

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Understanding how and why populations evolve is of fundamental importance to molecular ecology. Restriction site-associated DNA sequencing (RADseq), a popular reduced representation method, has ushered in a new era of genome-scale research for assessing population structure, hybridization, demographic history, phylogeography and migration. RADseq has also been widely used to conduct genome scans to detect loci involved in adaptive divergence among natural Correspondence: David B. Lowry, Fax: 517-353-1926; dlowry@msu.edu. Correction noteThe original advance online paper contained two errors associated with the calculation of the median density of RAD-seq tags in the survey of recent RAD-seq genome scan studies (Table S1). The first error was in the size of the assembled stickleback genome, which was reported as 0.53 Gbp, but should have been 0.46 Gbp. The second error was an accidental inversion of terms. These two mistakes contributed to an erroneous statement in the original abstract that the median density of RAD-tags across recent studies "was one marker per 3.96 megabases." The statement has been revised to read: "was 4.08 RAD-tag markers per megabase." Following these corrections, changes were made in the abstract and elsewhere in the paper to reflect a modified interpretation of the results, though we note the main arguments in the article are unaffected. Other minor modifications to the paper were made based upon suggestions by the editors of Molecular Ecology Resources. This version of the article, published as an "accepted article" on 12 November 2016 under DOI 10.1111/1755-0998.12635 replaces the original version of the article published on 12 September 2016 under DOI 10.1111/1755-0998.12596.The idea for the manuscript was conceived collectively by all authors during an NSF National Institute for Mathematical and Biological Synthesis (NIMBioS) working group. All authors contributed to the writing of the manuscript.Supporting Information Additional Supporting Information may be found in the online version of this article: Appendix S1 Supplementary R scripts for Breaking RAD. Table S1 Recent (January 2015 to April 2016) genome scan studies, which used RAD-seq for genotyping. Andrews et al. (2016). Generally, RADseq methods produce DNA libraries for high-throughput sequencing using restriction enzymes that cut at specific motifs throughout the genome. RADseq markers come in the form of RAD-tags, which are short-read sequences adjacent to restriction enzyme cut sites. Because many polymorphic markers are produced by RADseq, it has frequently been used successfully for population genetic analyses, including assessment of population structure, hybridization, demographic history, phylogeography and migration (Catchen et al. 2013;Cavender-Bares et al. 2015;Combosch & Vollmer 2015;Qi et al. 2015). Markers generated by RADseq have also been quite useful for constructing linkage maps and identifying quantitative trait loci (QTL;Pfender et al. 2011;Houston et al. 2012;Weber et al. 2013;Laporte et al. 2015...

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Population genomics of parallel hybrid zones in the mimetic butterflies,H. melpomeneandH. erato

Cited by 51 publications

References 83 publications

The Functional Basis of Wing Patterning inHeliconiusButterflies: The Molecules Behind Mimicry

The Functional Basis of Wing Patterning inHeliconiusButterflies: The Molecules Behind Mimicry

Coupling, Reinforcement, and Speciation

Breaking RAD: An evaluation of the utility of restriction site associated DNA sequencing for genome scans of adaptation

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