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Evolutionary novelty in a butterfly wing pattern through enhancer shuffling

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Wallbank, Richard W. R.
Baxter, Simon W.
Pardo Díaz, Geimy Carolina
Hanly, Joseph J.
Martin, Simon H.
Mallet, James
Dasmahapatra, Kanchon K.
Salazar, Camilo
Joron, Mathieu
Nadeau, Nicola



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An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation. © 2016 Wallbank et al.
Palabras clave
Alelos , Experimento con animales , Tejido animal , Mariposa , Estudio controlado , Región potenciadora , Miembro anterior , Gen , Regulación de la expresión génica , Locus de genes , Secuencia de genes , Cambio de genes , Recombinación genética , Variabilidad genética , Correlación de fenotipo genotipo , Heliconio elevado , Heliconio Melpomene , Hibridación , Genoma de insectos , Introgresión , Evolución Molecular , Filogenia molecular , No humano , Gen Optix , Identificación de especies , Genética , Fenotipo , Pigmentación , Evolución biológica
Animal , Biological Evolution , Pigmentation , Phenotype , Genetics , Species Identification , Optix Gene , Nonhuman , Molecular Phylogeny , Molecular Evolution , Introgression , Insect Genome , Hybridization , Heliconius Melpomene , Heliconius Elevatus , Genotype Phenotype Correlation , Genetic Variability , Genetic Recombination , Gene Switching , Gene Sequence , Gene Locus , Gene Expression Regulation , Gene , Forelimb , Enhancer Region , Controlled Study , Butterfly , Animal Tissue , Animal Experiment , Allele