Résumé
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.