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Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Accepted version
Peer-reviewed

Type

Article

Change log

Authors

Jiggins, CD 
Wallbank, RWR 
Hanly, JJ 

Abstract

A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis-regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.

This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

Description

Keywords

Lepidoptera, adaptive radiation, $\textit{cis}$-regulatory evolution, evo-devo, gene regulatory networks, mimicry

Journal Title

Philosophical Transactions of the Royal Society of London B: Biological Sciences

Conference Name

Journal ISSN

0962-8436
1471-2970

Volume Title

372

Publisher

Royal Society Publishing
Sponsorship
European Research Council (339873)
Leverhulme Trust (RPG-2014-167)
Wellcome Trust