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

Publication ,  Journal Article
Livraghi, L; Hanly, JJ; Evans, E; Wright, CJ; Loh, LS; Mazo-Vargas, A; Kamrava, K; Carter, A; van der Heijden, ESM; Reed, RD; Papa, R ...
Published in: Proceedings of the National Academy of Sciences of the United States of America
September 2024

Evolutionary variation in the wing pigmentation of butterflies and moths offers striking examples of adaptation by crypsis and mimicry. The cortex 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 ivory, transcribed from the cortex locus, in modulating color patterning in butterflies. Strikingly, ivory 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 ivory mutagenesis yields transformations of dark pigmented scales into white or light-colored scales. Genotyping of Vanessa cardui germline mutants associates these phenotypes to small on-target deletions at the conserved first exon of ivory. In contrast, cortex 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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Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

September 2024

Volume

121

Issue

36

Start / End Page

e2403326121

Related Subject Headings

  • Wings, Animal
  • RNA, Long Noncoding
  • Pigmentation
  • Phenotype
  • Butterflies
  • Animals
  • Adaptation, Physiological
 

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Livraghi, L., Hanly, J. J., Evans, E., Wright, C. J., Loh, L. S., Mazo-Vargas, A., … Martin, A. (2024). A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies. Proceedings of the National Academy of Sciences of the United States of America, 121(36), e2403326121. https://doi.org/10.1073/pnas.2403326121
Livraghi, Luca, Joseph J. Hanly, Elizabeth Evans, Charlotte J. Wright, Ling S. Loh, Anyi Mazo-Vargas, Kiana Kamrava, et al. “A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies.Proceedings of the National Academy of Sciences of the United States of America 121, no. 36 (September 2024): e2403326121. https://doi.org/10.1073/pnas.2403326121.
Livraghi L, Hanly JJ, Evans E, Wright CJ, Loh LS, Mazo-Vargas A, et al. A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies. Proceedings of the National Academy of Sciences of the United States of America. 2024 Sep;121(36):e2403326121.
Livraghi, Luca, et al. “A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies.Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 36, Sept. 2024, p. e2403326121. Epmc, doi:10.1073/pnas.2403326121.
Livraghi L, Hanly JJ, Evans E, Wright CJ, Loh LS, Mazo-Vargas A, Kamrava K, Carter A, van der Heijden ESM, Reed RD, Papa R, Jiggins CD, Martin A. A long noncoding RNA at the cortex locus controls adaptive coloration in butterflies. Proceedings of the National Academy of Sciences of the United States of America. 2024 Sep;121(36):e2403326121.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

September 2024

Volume

121

Issue

36

Start / End Page

e2403326121

Related Subject Headings

  • Wings, Animal
  • RNA, Long Noncoding
  • Pigmentation
  • Phenotype
  • Butterflies
  • Animals
  • Adaptation, Physiological