Evolutionary Novelty in a Butterfly Wing Pattern through Enhancer Shuffling.

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

doi:10.1371/journal.pbio.1002353

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.

Highlights

One of the major impediments to evolutionary innovation is the constraint on genetic change imposed by existing function [1]
Most of the 18,000 species of butterfly can be distinguished on the basis of their wing pattern
Despite the fact that they are part of a common pattern in the Amazon basin, these two pattern components arose in completely different species before being brought together through hybridisation. 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

Summary

Introduction

One of the major impediments to evolutionary innovation is the constraint on genetic change imposed by existing function [1]. Much of our understanding of modularity in regulatory evolution comes from Drosophila, in which the loss of trichomes on the larval cuticle [5], the gain of melanic wing spots [8,9,10], or changes in abdominal pigmentation [3,11] have been shown to involve evolutionary changes in cis-regulatory elements These elegant developmental studies demonstrate the underlying logic of regulatory modularity, whereby novel expression domains can arise without disrupting existing function. Similar conclusions come from recent work in other taxa, including mice and jewel wasps [2,12] This might seem to imply that the evolution of novel regulatory alleles is relatively gradual, requiring the evolution of many small effect substitutions, but recent adaptive radiations can show extremely rapid rates of morphological change. The role of regulatory modularity remains to be tested in adaptive radiations in which morphological variation evolves very rapidly

Methods

Results

Conclusion