A micro-RNA is the effector gene of a classic evolutionary hotspot locus

Tian, Shen; Asano, Yoshimasa; Banerjee, Tirtha Das; Wee, Jocelyn Liang Qi; Lamb, Abigail; Wang, Yehan; Murugesan, Suriya Narayanan; Ui-Tei, Kumiko; Wittkopp, Patricia J; Monteiro, Antonia

doi:10.1101/2024.02.09.579741

Cited by 3 publications

References 51 publications

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The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

Fandino,

Brady,

Chatterjee

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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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, 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 noncoding RNA can exert diverse and nuanced effects on the evolution and development of color patterns, including modulating seasonally plastic color patterns.

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The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

Fandino,

Brady,

Chatterjee

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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TheivorylncRNA regulates seasonal color patterns in buckeye butterflies

Fandino,

Brady,

Chatterjee

et al. 2024

Preprint

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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 the Livraghi et. al companion paper, 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.

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Lepidopteran scale cells derive from sensory organ precursors through a canonical lineage

Loh,

DeMarr,

Tsimba

et al. 2024

Preprint

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The success of butterflies and moths is tightly linked to the origin of scales within the group. A long-standing hypothesis postulates that scales are homologous to the well-described mechanosensory bristles found in the fruit flyDrosophila melanogaster, where both derive from an epithelial precursor specified by lateral inhibition that then undergoes multiple rounds of division. Previous histological examination and candidate gene approaches identified parallels in genes involved in scale and bristle development. Here, we provide definitive developmental and transcriptomic evidence that the differentiation of lepidopteran scales derives from the canonical cell lineage, known as the Sensory Organ Precursor (SOP). Live imaging in moth and butterfly pupae shows that SOP cells undergo two rounds of asymmetric divisions that first abrogate the neurogenic lineage, and then lead to a differentiated scale precursor and its associated socket cell. Single-nucleus RNA sequencing across a time-series of early pupal development revealed differential gene expression patterns that mirror canonical lineage development, including Notch-Delta signalling components, cell adhesion molecules, cell cycling factors, and terminal cell differentiation markers, suggesting a shared origin of the SOP developmental program. Additionally, we recovered a novel gene, the POU-domain transcription factorpdm3, involved in the proper differentiation of butterfly wing scales. Altogether, these data open up avenues for understanding scale type specification and development, and illustrate how single-cell transcriptomics provide a powerful platform for understanding the evolution of cell types.

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A micro-RNA is the effector gene of a classic evolutionary hotspot locus

Cited by 3 publications

References 51 publications

The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

The ivory lncRNA regulates seasonal color patterns in buckeye butterflies

TheivorylncRNA regulates seasonal color patterns in buckeye butterflies

Lepidopteran scale cells derive from sensory organ precursors through a canonical lineage

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