The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

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Abstract Long non-coding RNAs (lncRNAs) are transcribed elements increasingly recognized for their roles in regulating gene expression. Thus far, however, we have little understanding of how lncRNAs contribute to evolution and adaptation. Here we show that a conserved lncRNA, ivory , is an important color patterning gene in the buckeye butterfly Junonia coenia . ivory overlaps with cortex , a locus linked to multiple cases of crypsis and mimicry in Lepidoptera. Along with a companion paper by Livraghi et. al., we argue that ivory , not cortex , is the color pattern gene of interest at this locus. In J. coenia a cluster of cis -regulatory elements (CREs) in the first intron of ivory are genetically associated with natural variation in seasonal color pattern plasticity, and targeted deletions of these CREs phenocopy seasonal phenotypes. Deletions of different ivory CREs produce other distinct phenotypes as well, including loss of melanic eyespot rings, and positive and negative changes in overall wing pigmentation. We show that the color pattern transcription factors Spineless, Bric-a-brac, and Ftz-f1 bind to the ivory promoter during wing pattern development, suggesting that they directly regulate ivory . This case study demonstrates how cis -regulation of a single non-coding RNA can exert diverse and nuanced effects on the evolution and development of color patterns, including modulating seasonally plastic color patterns. Significance The genomic locus hosting the cortex gene has been linked to numerous cases of color pattern adaptation in moths and butterflies, including crypsis, mimicry, and seasonal polyphenism. Here we show in buckeye butterflies that the actual color pattern gene at the cortex locus is an evolutionarily conserved long non-coding RNA (lncRNA), dubbed ivory , that overlaps with cortex . Compared with other wing pattern genes, ivory stands out because of the highly nuanced, quantitative changes in pigmentation that can be achieved by manipulating adjacent cis -regulatory sequences. This study highlights how lncRNAs can be important factors underlying morphological evolution, and emphasizes the importance of considering non-coding transcripts in comparative genomics.

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