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Development Genes and Evolution

, Volume 221, Issue 5–6, pp 297–308 | Cite as

Convergent, modular expression of ebony and tan in the mimetic wing patterns of Heliconius butterflies

  • Laura C. Ferguson
  • Luana Maroja
  • Chris D. JigginsEmail author
Original Article

Abstract

The evolution of pigmentation in vertebrates and flies has involved repeated divergence at a small number of genes related to melanin synthesis. Here, we study insect melanin synthesis genes in Heliconius butterflies, a group characterised by its diversity of wing patterns consisting of black (melanin), and yellow and red (ommochrome) pigmented scales. Consistent with their respective biochemical roles in Drosophila melanogaster, ebony is upregulated in non-melanic wing regions destined to be pigmented red whilst tan is upregulated in melanic regions. Wing regions destined to be pigmented yellow, however, are downregulated for both genes. This pattern is conserved across multiple divergent and convergent phenotypes within the Heliconii, suggesting a conserved mechanism for the development of black, red and yellow pattern elements across the genus. Linkage mapping of five melanin biosynthesis genes showed that, in contrast to other organisms, these genes do not control pattern polymorphism. Thus, the pigmentation genes themselves are not the locus of evolutionary change but lie downstream of a wing pattern regulatory factor. The results suggest a modular system in which particular combinations of genes are switched on whenever red, yellow or black pattern elements are favoured by natural selection for diverse and mimetic wing patterns.

Keywords

Pigmentation Heliconius Ebony Tan Mimicry 

Notes

Acknowledgements

We thank Nick Mundy for the use of his qRT-PCR machine, and Simon Baxter and Claire Webster for contributing to linkage mapping. Breeding was carried out with assistance from R. Merrill, and Moises Abanto. Ana Portugal and Grace Wu assisted with dissections. This work was funded by a NERC Ph.D. Studentship to L. Ferguson, BBSRC support of L. Maroja and Leverhulme Trust Research Leadership grant and a Royal Society Fellowship to C. Jiggins.

Supplementary material

427_2011_380_Fig5_ESM.jpg (103 kb)
Supplementary Fig. 1

Increased resolution of melanic staging for the Heliconius. As melanogenesis is rapid in H. melpomene (e.g. approximately 30 min, separate the early and mid-melanic stages), we increased the resolution of developmental staging around melanisation to reduce variability between biological replicates. From dissection of 117 individuals, the early melanin stage was divided into three and the mid-melanin stage into five. EM1 hint of melanic pigment in distal portion of the wing, EM2 pale melanic pigment in distal portion of the wing, EM3 dark melanic pigment in distal portion of the wing, MM1 pale melanic pigment in proximal portion of the wing, MM2 dark melanic pigment in proximal portion of the wing, MM3 few veins pigmented in distal portion of the wing, MM4 most veins pigmented in distal portion of the wing, MM5 all veins pigmented in distal portion of the wing. Only wings from mid-melanin stages 1–3 were used for further qRT-PCR. (JPEG 103 kb)

427_2011_380_MOESM1_ESM.tif (8.7 mb)
High-resolution image (TIFF 8921 kb)
427_2011_380_Fig6_ESM.jpg (57 kb)
Supplementary Fig. 2

Example of dissected regions for comparative qRT-PCR. Individuals shown were included in the replicates used (JPEG 57 kb)

427_2011_380_MOESM2_ESM.tif (2.2 mb)
High-resolution image (TIFF 2211 kb)
427_2011_380_MOESM3_ESM.doc (40 kb)
Supplementary Table 1 Maximum expression levels of pigmentation genes relative to the control as recorded by qRT-PCR (DOC 39 kb)

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Laura C. Ferguson
    • 1
    • 2
  • Luana Maroja
    • 3
  • Chris D. Jiggins
    • 1
    Email author
  1. 1.Department of ZoologyUniversity of CambridgeCambridgeUK
  2. 2.Department of ZoologyUniversity of OxfordOxfordUK
  3. 3.Biology Department, Thompson Biology LaboratoryWilliams CollegeWilliamstownUSA

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