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

Abstract

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 fly Drosophila melanogaster, as both derive from an epithelial precursor. Previous histological and candidate gene approaches identified parallels in genes involved in scale and bristle development. Here, we provide developmental and transcriptomic evidence that the differentiation of lepidopteran scales derives from the sensory organ precursor (SOP). Live imaging in lepidopteran pupae shows that SOP cells undergo two 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 using early pupal wings revealed differential gene expression patterns that mirror SOP development, suggesting a shared developmental program. Additionally, we recovered a newly associated gene, the transcription factor pdm3, 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 evolution of cell types.