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Type: Journal article
Title: Genomic hotspots for adaptation: the population genetics of Müllerian mimicry in the Heliconius melpomene clade
Other Titles: Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in the Heliconius melpomene clade
Author: Baxter, S.
Nadeau, N.
Maroja, L.
Wilkinson, P.
Counterman, B.
Dawson, A.
Beltran, M.
Perez-Espona, S.
Chamberlain, N.
Ferguson, L.
Clark, R.
Davidson, C.
Glithero, R.
Mallet, J.
McMillan, W.
Kronforst, M.
Joron, M.
ffrench-Constant, R.
Jiggins, C.
Citation: PLoS Genetics, 2010; 6(2):1-13
Publisher: Public Library of Science
Issue Date: 2010
ISSN: 1553-7390
Statement of
Simon 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
Abstract: Wing 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.
Keywords: Chromosomes, Artificial, Bacterial; Animals; Butterflies; Insect Proteins; Genetics, Population; Population Dynamics; Adaptation, Physiological; Phylogeny; Species Specificity; Gene Expression Regulation; Molecular Mimicry; Genotype; Linkage Disequilibrium; Phenotype; Genes, Insect; Genome; Genetic Variation; Selection, Genetic; Genetic Loci
Rights: Copyright © 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.
RMID: 0020123870
DOI: 10.1371/journal.pgen.1000794
Appears in Collections:Molecular and Biomedical Science publications
Environment Institute publications

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