Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade

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dc.contributor.authorBaxter, S.
dc.contributor.authorNadeau, N.
dc.contributor.authorMaroja, L.
dc.contributor.authorWilkinson, P.
dc.contributor.authorCounterman, B.
dc.contributor.authorDawson, A.
dc.contributor.authorBeltran, M.
dc.contributor.authorPerez-Espona, S.
dc.contributor.authorChamberlain, N.
dc.contributor.authorFerguson, L.
dc.contributor.authorClark, R.
dc.contributor.authorDavidson, C.
dc.contributor.authorGlithero, R.
dc.contributor.authorMallet, J.
dc.contributor.authorMcMillan, W.
dc.contributor.authorKronforst, M.
dc.contributor.authorJoron, M.
dc.contributor.authorffrench-Constant, R.
dc.contributor.authorJiggins, C.
dc.contributor.editorNachman, M.W.
dc.date.issued2010
dc.description.abstractWing patterning in Heliconius butterflies is a longstanding example of both Müllerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are “hotspots” for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by ~100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Müllerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.
dc.description.statementofresponsibilitySimon W. Baxter, Nicola J. Nadeau, Luana S. Maroja, Paul Wilkinson, Brian A. Coutnerman, Anna Dawson, Margarita Beltran, Silvia Perez-Espona, Nicola Chamberlain, Laura Ferguson, Richard Clark, Claire Davidson, Rebecca Glithero, James Mallett, W. Owen McMillan, Marcus Kronforst, Mathieu Joron, Richard H. ffrench-Constant and Chris D. Jiggins
dc.identifier.citationPLoS Genetics, 2010; 6(2):1-13
dc.identifier.doi10.1371/journal.pgen.1000794
dc.identifier.issn1553-7390
dc.identifier.issn1553-7404
dc.identifier.orcidBaxter, S. [0000-0001-5773-6578]
dc.identifier.orcidDawson, A. [0000-0002-9347-0540]
dc.identifier.urihttp://hdl.handle.net/2440/76582
dc.language.isoen
dc.publisherPublic Library of Science
dc.rightsCopyright © 2010 Baxter et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
dc.source.urihttps://doi.org/10.1371/journal.pgen.1000794
dc.subjectChromosomes, Artificial, Bacterial
dc.subjectAnimals
dc.subjectButterflies
dc.subjectInsect Proteins
dc.subjectGenetics, Population
dc.subjectPopulation Dynamics
dc.subjectAdaptation, Physiological
dc.subjectPhylogeny
dc.subjectSpecies Specificity
dc.subjectGene Expression Regulation
dc.subjectMolecular Mimicry
dc.subjectGenotype
dc.subjectLinkage Disequilibrium
dc.subjectPhenotype
dc.subjectGenes, Insect
dc.subjectGenome
dc.subjectGenetic Variation
dc.subjectSelection, Genetic
dc.subjectGenetic Loci
dc.titleGenomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade
dc.title.alternativeGenomic hotspots for adaptation: the population genetics of Mullerian mimicry in the Heliconius melpomene clade
dc.typeJournal article
pubs.publication-statusPublished

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