A single-cell atlas of the sexually dimorphic Drosophila foreleg and its sensory organs during development

Abstract

To respond to the world around them, animals rely on the input of a network of sensory organs distributed throughout the body. Distinct classes of sensory organs are specialized for the detection of specific stimuli such as strain, pressure, or taste. The features that underlie this specialization relate both to the neurons that innervate sensory organs and the accessory cells they comprise. To understand the genetic basis of this diversity of cell types, both within and between sensory organs, we performed single-cell RNA sequencing on the first tarsal segment of the male Drosophila melanogaster foreleg during pupal development. This tissue displays a wide variety of functionally and structurally distinct sensory organs, including campaniform sensilla, mechanosensory bristles, and chemosensory taste bristles, as well as the sex comb, a recently evolved male-specific structure. In this study, we characterize the cellular landscape in which the sensory organs reside, identify a novel cell type that contributes to the construction of the neural lamella, and resolve the transcriptomic differences among support cells within and between sensory organs. We identify the genes that distinguish between mechanosensory and chemosensory neurons, resolve a combinatorial transcription factor code that defines 4 distinct classes of gustatory neurons and several types of mechanosensory neurons, and match the expression of sensory receptor genes to specific neuron classes. Collectively, our work identifies core genetic features of a variety of sensory organs and provides a rich, annotated resource for studying their development and function.

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

“…Expression of ss was restricted to scale-building cells similar to sv (Figure 3I). Within the same cluster scale-building cell, additional marker genes include CG14395, part of the gene regulatory network (GRN) including shavenbaby/ovo; the gene shavenoid (sha), also found in Hopkins et al (2023). Cluster scale-building cell also expressed genes for transcription factors ichor (ich) and couch potato (cpo), the latter which was also identified in Prakash et al (2024) and we confirmed its expression in scale-building cells by HCR (Figure 3J).…”

“…Cluster scale-building cell also expressed genes for transcription factors ichor (ich) and couch potato (cpo), the latter which was also identified in Prakash et al (2024) and we confirmed its expression in scale-building cells by HCR (Figure 3J). Cytoskeletal gene quail (qua) and the lncRNA ivory, responsible for the normal development of scale colour, were identified as well (Hopkins et al, 2023;Kittelmann et al, 2018;Livraghi et al, 2024;Prakash et al, 2024). Osiris4 (Osi4), a member of the insect-specific Osiris family of genes recently found to be expressed in a variety of Drosophila macrochaetae, was also restricted to the scale-building cell cluster (Sun et al, 2024).…”

“…D. melanogaster SOP derivatives follow a stereotyped pattern of division and differentiation, guided by a conserved gene regulatory network (Figure 1A). Variations from the canonical lineage result in morphologically distinct sensory organs, with modifications including lineage-specific cell proliferation or death, novel recruitment into the sensory cluster and the alteration of the terminal progenitor cell fates (Hopkins et al, 2023; Klann et al, 2021; Mangione et al, 2023).…”

“… A-B. A comparative depiction of the canonical SOP lineage in D. melanogaster [A; adapted from Hopkins et al . (2023)], and the hypothetical lineage of lepidopteran wing scales (B), where pIIb and its derivatives are missing or not observed in histology and live imaging records (Ghiradella, 1998; McDougal et al, 2021; Stossberg, 1938).…”

Insect Insights at the Single-Cell Level: Technologies and Applications

“…A number of single-cell transcriptome studies have been conducted to explore the complexity of insect nervous systems (See Table 1 ). Unlike the peripheral nervous system and sympathetic nervous system, which have received negligible attention with few related publications [ 101 ], the majority of research on insect nervous systems is focused on the central nervous system (CNS).…”