Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids

• Published in: Nature communications Vol. 15; no. 1; p. 1047
• Main Authors: Bontonou, Gwénaëlle, Saint-Leandre, Bastien, Kafle, Tane, Baticle, Tess, Hassan, Afrah, Sánchez-Alcañiz, Juan Antonio, Arguello, J. Roman
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 05-02-2024; Nature Publishing Group; Nature Portfolio
• Subjects: 14; 14/19; 14/32; 38; 38/39; 45; 631/1647/334/1582/715; 631/181/2474; 631/378/3917; 631/61/191/2018; 64; 64/24; Animals; Chemoreception; Chemoreceptors; Drosophila; Drosophila - genetics; Drosophila - metabolism; Drosophila melanogaster - genetics; Drosophila melanogaster - metabolism; Drosophila Proteins - genetics; Drosophila Proteins - metabolism; Evolution; Evolution, Molecular; Female; Fruit flies; Gene expression; Gene Expression Profiling; Genes; Humanities and Social Sciences; Insects; Male; multidisciplinary; Phylogeny; Science; Science (multidisciplinary); Sex differences; Species; Tissues; Transcriptome; Transcriptomes; Transcriptomics
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-44558-4

Chemosensory tissues exhibit significant between-species variability, yet the evolution of gene expression and cell types underlying this diversity remain poorly understood. To address these questions, we conducted transcriptomic analyses of five chemosensory tissues from six
Drosophila
species and integrated the findings with single-cell datasets. While stabilizing selection predominantly shapes chemosensory transcriptomes, thousands of genes in each tissue have evolved expression differences. Genes that have changed expression in one tissue have often changed in multiple other tissues but at different past epochs and are more likely to be cell type-specific than unchanged genes. Notably, chemosensory-related genes have undergone widespread expression changes, with numerous species-specific gains/losses including novel chemoreceptors expression patterns. Sex differences are also pervasive, including a
D. melanogaster-
specific excess of male-biased expression in sensory and muscle cells in its forelegs. Together, our analyses provide new insights for understanding evolutionary changes in chemosensory tissues at both global and individual gene levels.
Chemosensory tissues are remarkably variable between species but the cause of this diversity is unclear. Here, the authors conduct transcriptomic analyses of chemosensory tissues from diverse
Drosophila
species, revealing evidence of stabilizing selection and recent species- and sex-specific changes.