A long noncoding RNA at the <i>cortex</i> locus controls adaptive coloration in butterflies

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The <i>cortex</i> locus has been independently mapped as the locus controlling color polymorphisms in 15 lepidopteran species, suggesting that it acts as a genomic hotspot for the diversification of wing patterns, but functional validation through protein-coding knockouts has proven difficult to obtain. Our study unveils the role of a long noncoding RNA (lncRNA) which we name <i>ivory</i>, transcribed from the <i>cortex</i> locus, in modulating color patterning in butterflies. Strikingly, <i>ivory</i> expression prefigures most melanic patterns during pupal development, suggesting an early developmental role in specifying scale identity. To test this, we generated CRISPR mosaic knock-outs in five nymphalid butterfly species and show that <i>ivory</i> mutagenesis yields transformations of dark pigmented scales into white or light-colored scales. Genotyping of <i>Vanessa cardui</i> germline mutants associates these phenotypes to small on-target deletions at the conserved first exon of <i>ivory</i>. In contrast, <i>cortex</i> germline mutant butterflies with confirmed null alleles lack any wing phenotype and exclude a color patterning role for this adjacent gene. Overall, these results show that a lncRNA gene acts as a master switch of color pattern specification and played key roles in the adaptive diversification of wing patterns in butterflies.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-08-30
DOI
https://doi.org/10.1073/pnas.2403326121
Citations
24
Primary Topic
Lepidoptera: Biology and Taxonomy
Type
article
Field-Weighted Citation Impact
13.21

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article

A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies

Eva S. M. van der Heijden, Robert D. Reed, Ling S. Loh, Alexander Carter et al.
24 citations
Proceedings of the National Academy of Sciences
Lepidoptera: Biology and Taxonomy
13.21
article

A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies

Eva S. M. van der Heijden, Robert D. Reed, Ling S. Loh, Alexander Carter, Arnaud Martin, Chris D. Jiggins, Luca Livraghi, Joseph J. Hanly, Charlotte J Wright, Riccardo Papa, Anyi Mazo‐Vargas, Kiana Kamrava, Elizabeth Evans
article en
24 citations

Abstract

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The <i>cortex</i> locus has been independently mapped as the locus controlling color polymorphisms in 15 lepidopteran species, suggesting that it acts as a genomic hotspot for the diversification of wing patterns, but functional validation through protein-coding knockouts has proven difficult to obtain. Our study unveils the role of a long noncoding RNA (lncRNA) which we name <i>ivory</i>, transcribed from the <i>cortex</i> locus, in modulating color patterning in butterflies. Strikingly, <i>ivory</i> expression prefigures most melanic patterns during pupal development, suggesting an early developmental role in specifying scale identity. To test this, we generated CRISPR mosaic knock-outs in five nymphalid butterfly species and show that <i>ivory</i> mutagenesis yields transformations of dark pigmented scales into white or light-colored scales. Genotyping of <i>Vanessa cardui</i> germline mutants associates these phenotypes to small on-target deletions at the conserved first exon of <i>ivory</i>. In contrast, <i>cortex</i> germline mutant butterflies with confirmed null alleles lack any wing phenotype and exclude a color patterning role for this adjacent gene. Overall, these results show that a lncRNA gene acts as a master switch of color pattern specification and played key roles in the adaptive diversification of wing patterns in butterflies.

Proceedings of the National Academy of SciencesVol. 121(36)
University of Parma (IT), Smithsonian Tropical Research Institute (PA), University of Puerto Rico at Río Piedras (PR), Duke University (US), George Washington University (US), University of Puerto Rico System (PR), Cornell University (US), University of Cambridge (GB), Wellcome Sanger Institute (GB)
National Science Foundation, Smithsonian Institution, George Washington University, Università degli Studi di Parma, Puerto Rico Science, Technology and Research Trust, Directorate for Biological Sciences, Smithsonian Tropical Research Institute, Department of Biology, Duke University, Biotechnology and Biological Sciences Research Council, Division of Integrative Organismal Systems, Office of Experimental Program to Stimulate Competitive Research
Life in Land
Openalex Percentile: Top 1%
Lepidoptera: Biology and Taxonomy
13.21
DOIOpen Access PDFOpenAlex
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