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Open Access Research article

Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation

Heather M Hines12*, Riccardo Papa34, Mayte Ruiz4, Alexie Papanicolaou5, Charles Wang6, H Frederik Nijhout7, W Owen McMillan18 and Robert D Reed389

  • * Corresponding author: Heather M Hines hmh19@psu.edu

  • † Equal contributors

Author Affiliations

1 Department of Genetics, North Carolina State University, Raleigh, NC, 27695, USA

2 Department of Biology, Pennsylvania State University, University Park, PA, 16802, USA

3 Department of Ecology and Evolutionary Biology, University of California, Irvine, CA, 92697, USA

4 Department of Biology and Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, San Juan, Puerto Rico, 00921

5 CSIRO Ecosystem Sciences, GPO 1700, Canberra, ACT, 2601, Australia

6 Functional Genomics Core, Beckman Research Institute, City of Hope, Duarte, CA, 91010, USA

7 Department of Biology, Duke University, Durham, NC, 27708, USA

8 Smithsonian Tropical Research Institute, Panama City, Panama

9 Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA

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BMC Genomics 2012, 13:288  doi:10.1186/1471-2164-13-288

Published: 29 June 2012

Abstract

Background

Heliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes. Positional cloning and candidate gene studies have identified a handful of regulatory and pigmentation genes implicated in Heliconius wing pattern variation, but little is known about the greater developmental networks within which these genes interact to pattern a wing. Here we took a large-scale transcriptomic approach to identify the network of genes involved in Heliconius wing pattern development and variation. This included applying over 140 transcriptome microarrays to assay gene expression in dissected wing pattern elements across a range of developmental stages and wing pattern morphs of Heliconius erato.

Results

We identified a number of putative early prepattern genes with color-pattern related expression domains. We also identified 51 genes differentially expressed in association with natural color pattern variation. Of these, the previously identified color pattern “switch gene” optix was recovered as the first transcript to show color-specific differential expression. Most differentially expressed genes were transcribed late in pupal development and have roles in cuticle formation or pigment synthesis. These include previously undescribed transporter genes associated with ommochrome pigmentation. Furthermore, we observed upregulation of melanin-repressing genes such as ebony and Dat1 in non-melanic patterns.

Conclusions

This study identifies many new genes implicated in butterfly wing pattern development and provides a glimpse into the number and types of genes affected by variation in genes that drive color pattern evolution.

Keywords:
Heliconius; Adaptation; Pigmentation; Ommochrome; Melanin; Genomics; Evo-devo