Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations

Arnaud Martin, Kyle J. McCulloch, Nipam H. Patel, Adriana D. Briscoe, Lawrence E. Gilbert, Robert D. Reed

Research output: Contribution to journalArticlepeer-review

63 Scopus citations


Background: While the ecological factors that drive phenotypic radiations are often well understood, less is known about the generative mechanisms that cause the emergence and subsequent diversification of novel features. Heliconius butterflies display an extraordinary diversity of wing patterns due in part to mimicry and sexual selection. Identifying the genetic drivers of this crucible of evolution is now within reach, as it was recently shown that cis-regulatory variation of the optix transcription factor explains red pattern differences in the adaptive radiations of the Heliconius melpomene and Heliconius erato species groups.Results: Here, we compare the developmental expression of the Optix protein across a large phylogenetic sample of butterflies and infer that its color patterning role originated at the base of the neotropical passion-vine butterfly clade (Lepidoptera, Nymphalidae, Tribe: Heliconiini), shortly predating multiple Optix-driven wing pattern radiations in the speciose Heliconius and Eueides genera. We also characterize novel Optix and Doublesex expression in the male-specific pheromone wing scales of the basal heliconiines Dryas and Agraulis, thus illustrating that within the Heliconinii lineage, Optix has been evolutionarily redeployed in multiple contexts in association with diverse wing features.Conclusions: Our findings reveal that the repeated co-option of Optix into various aspects of wing scale specification was associated with multiple evolutionary novelties over a relatively short evolutionary time scale. In particular, the recruitment of Optix expression in colored scale cell precursors was a necessary condition to the explosive diversification of passion-vine butterfly wing patterns. The novel deployment of a gene followed by spatial modulation of its expression in a given cell type could be a common mode of developmental innovation for triggering phenotypic radiations.

Original languageEnglish (US)
Article number7
Issue number1
StatePublished - Feb 5 2014
Externally publishedYes

Bibliographical note

Funding Information:
We are grateful to Angela Kaczmarczyk for helping with recombinant protein purification, Carmen Robinett for sharing the anti-Doublesex antibody, and Theresa Freiburger for butterfly husbandry at UT Austin. Thomas Schilling provided continuous support for this research and we also thank the members of his laboratory for technical assistance and fruitful discussions. This work was supported by the National Science Foundation grant IOS-1052541 to RDR.


  • Adaptive radiation
  • Co-option
  • Evolutionary novelty
  • Heliconius
  • Pattern evolution
  • Sexual dimorphism


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