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Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling

Richard W. R. Wallbank , Simon W. Baxter , Carolina Pardo-Diaz, Joseph J. Hanly, Simon H. Martin, James Mallet, Kanchon K. Dasmahapatra, Camilo Salazar, Mathieu Joron, Nicola Nadeau, W. Owen McMillan, Chris D. Jiggins 

Published: January 15, 2016DOI: 10.1371/journal.pbio.1002353

Fig 1. Diversity of the Amazonian dennis-ray mimicry ring.


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.

Author Summary

Butterflies show an amazing diversity of patterns on their wings. In fact, most of the 18,000 species of butterfly can be distinguished on the basis of their wing pattern. Much of this diversity is thought to arise through novel switches in the genome that turn genes on in new contexts during wing development, thereby producing new patterns. Here we study a set of switches that control the expression of optix, a gene that places red patches onto the wings of Heliconius butterflies. We show that two patterning switches—one that produces red rays on the hindwing and the other a red patch on the base of the forewing—are located adjacent to one another in the genome. These switches have each evolved just once among a group of 16 species but have then been repeatedly shared between species by hybridisation and introgression. Despite the fact that they are now part of a common pattern in the Amazon basin, these two pattern components actually arose in completely different species before being brought together through hybridisation. In addition, recombination among these switches has produced new combinations of patterns within species. Such sharing of genetic variation is one way in which mimicry can evolve, whereby patterns are shared between species to send a common signal to predators. Our work suggests a new mechanism for generating evolutionary novelty, by shuffling these genetic switches among lineages and within species.

Citation: Wallbank RWR, Baxter SW, Pardo-Diaz C, Hanly JJ, Martin SH, Mallet J, et al. (2016) Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling. PLoS Biol 14(1): e1002353. doi:10.1371/journal.pbio.1002353

Academic Editor: Nick H. Barton, Institute of Science and Technology Austria (IST Austria), AUSTRIA

Received: June 17, 2015; Accepted: December 8, 2015; Published: January 15, 2016

Copyright: © 2016 Wallbank 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.

Data Availability: All complete genome sequence data are available through the Short Read Archive with project accession number ERP009041 (full details in Samples S3 Table). The sequence alignment, association data and other raw data are available on DataDryad http://dx.doi.org/10.5061/dryad.t3r02.

Funding: This study was funded by the Biotechnology and Biological Sciences Research Council http://www.bbsrc.ac.uk grant number H01439X/1 to CDJ; the European Research Council MimEvol grant to MJ and the European Research Council Speciation Genetics to CDJ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Abbreviations: BLAST, Basic Local Alignment Search Tool; HPD, highest posterior density; ML, maximum likelihood; SNP, single nucleotide polymorphism