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PLoS Biol. 2016 Jan 15;14(1):e1002353. doi: 10.1371/journal.pbio.1002353. eCollection 2016 Jan.

Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.

Author information

Department of Zoology, University of Cambridge, Cambridge, United Kingdom.
Smithsonian Tropical Research Institution, Balboa, Ancón, Panama.
School of Biological Sciences, University of Adelaide, Adelaide, Australia.
Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Bogotá, D.C., Colombia.
Organismic and Evolutionary Biology, Harvard University, Harvard, Massachusetts, United States of America.
Department of Biology, University of York, York, United Kingdom.
Institut de Systématique Evolution et Biodiversité, UMR 7205, CNRS MNHN UPMC EPHE, Muséum National d'Histoire Naturelle, CP50, Paris, France.
Centre d'Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS-Université de Montpellier-Université Paul-Valéry-EPHE, Montpellier, France.
Dept. of Animal and Plant Sciences, University of Sheffield, Sheffield, United Kingdom.


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.

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