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Edited by Sean B. Carroll, Howard Hughes Medical Institute and University of Wisconsin–Madison, Madison, WI, and approved August 1, 2017 (received for review May 31, 2017)
Significance
The optix gene is well known for its genetic association with wing pattern variation in butterflies; however, its actual function has never been directly confirmed. Using CRISPR genome editing in multiple butterfly species, we show that this gene plays a fundamental and deeply conserved role in the butterfly family Nymphalidae, where it acts as an activator of wing color. We were also surprised to discover that optix simultaneously controls blue iridescence in some species as well, providing an example of how a single gene can act as a switch to coordinate between structural and pigmentary coloration.
Abstract
The optix gene has been implicated in butterfly wing pattern adaptation by genetic association, mapping, and expression studies. The actual developmental function of this gene has remained unclear, however. Here we used CRISPR/Cas9 genome editing to show that optix plays a fundamental role in nymphalid butterfly wing pattern development, where it is required for determination of all chromatic coloration. optix knockouts in four species show complete replacement of color pigments with melanins, with corresponding changes in pigment-related gene expression, resulting in black and gray butterflies. We also show that optix simultaneously acts as a switch gene for blue structural iridescence in some butterflies, demonstrating simple regulatory coordination of structural and pigmentary coloration. Remarkably, these optix knockouts phenocopy the recurring “black and blue” wing pattern archetype that has arisen on many independent occasions in butterflies. Here we demonstrate a simple genetic basis for structural coloration, and show that optix plays a deeply conserved role in butterfly wing pattern development.
Footnotes
- ↵1To whom correspondence should be addressed. Email: robertreed{at}cornell.edu.
Author contributions: L.Z. and R.D.R. designed research; L.Z. and A.M.-V. performed research; L.Z. analyzed data; and L.Z. and R.D.R. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The data reported in this paper have been deposited in the Gene Expression Omnibus (GEO) database, https://www.ncbi.nlm.nih.gov/geo (accession no. GSE98678).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1709058114/-/DCSupplemental.
Genetic basis of butterfly color and iridescence
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