@article {798186, title = {The origins of an evolutionary novelty through enhancer shuffling}, journal = {PloS Biology}, volume = {14}, year = {2016}, note = {OPEN ACCESS}, pages = {e1002353}, abstract = {

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 = {Wallbank, R.W.R. and Baxter, S. and Pardo-Diaz, C. and Hanly, J.J. and Martin, S. H. and Mallet, J. and Dasmahapatra, K. K. and Salazar, C. and Joron, M. and Nadeau, N. and McMillan, W. O. and Jiggins, C. D.} }