The <i>ivory</i> lncRNA regulates seasonal color patterns in buckeye butterflies.

Abstract

Long noncoding 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, <i>ivory</i>, is an important color patterning gene in the buckeye butterfly <i>Junonia coenia</i>. <i>ivory</i> overlaps with <i>cortex</i>, a locus linked to multiple cases of crypsis and mimicry in Lepidoptera. Along with a companion paper by Livraghi et al., we argue that <i>ivory</i>, not <i>cortex</i>, is the color pattern gene of interest at this locus. In <i>J. coenia</i>, a cluster of <i>cis</i>-regulatory elements (CREs) in the first intron of <i>ivory</i> are genetically associated with natural variation in seasonal color pattern plasticity, and targeted deletions of these CREs phenocopy seasonal phenotypes. Deletions of different <i>ivory</i> 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 <i>ivory</i> promoter during wing pattern development, suggesting that they directly regulate <i>ivory</i>. This case study demonstrates how <i>cis</i>-regulation of a single noncoding RNA can exert diverse and nuanced effects on the evolution and development of color patterns, including modulating seasonally plastic color patterns.