High-resolution single-cell analyses reveal evolutionary constraints and evolvability of sexual circuits in Drosophila

Understanding how the cellular and molecular composition of neural circuits evolves to generate species-specific behaviors remains a major challenge in evolutionary biology and neuroscience. The remarkable diversity of male sexual behaviors among species, despite their recent divergence, offers an e...

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Published in:Proceedings of the National Academy of Sciences - PNAS Vol. 122; no. 47; p. e2516083122
Main Authors: Walsh, Justin T, Junker, Ian P, Chen, Yu-Chieh David, Chen, Yen-Chung, Gifford, Helena, Chen, Dawn S, Ding, Yun
Format: Journal Article
Language:English
Published: United States 25.11.2025
Subjects:
Animals
Biological Evolution
DNA-Binding Proteins - genetics
DNA-Binding Proteins - metabolism
Drosophila - genetics
Drosophila - physiology
Drosophila melanogaster - genetics
Drosophila melanogaster - physiology
Drosophila Proteins - genetics
Drosophila Proteins - metabolism
Evolution, Molecular
Female
Male
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
Neurons - metabolism
Sexual Behavior, Animal - physiology
Single-Cell Analysis - methods
Transcription Factors - genetics
Transcription Factors - metabolism
Transcriptome
evolution of cell types
single-cell transcriptomics
behavioral evolution
neural circuit evolution
neuropeptide signaling
ISSN:1091-6490, 1091-6490
Online Access:Get more information
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Summary:Understanding how the cellular and molecular composition of neural circuits evolves to generate species-specific behaviors remains a major challenge in evolutionary biology and neuroscience. The remarkable diversity of male sexual behaviors among species, despite their recent divergence, offers an excellent model for addressing this question. Here, by harnessing single-cell transcriptomics of the sexual circuits labeled by the sex determination gene ( ) at high resolution, we delineated 84 molecularly distinct + cell types, each mapped to anatomically and functionally defined + neural populations. Our findings revealed a largely conserved cellular architecture, with minimal evolutionary gain or loss of cell types across four species. A detailed comparison between ( ) and uncovered pervasive heterogeneity in transcriptomic divergence among + cell types. While core cell type identities-defined by the sex determination gene ( ), neurotransmitters, monoamines, and transcription factors-remain highly conserved, we observed striking evolutionary turnover in neuropeptide signaling pathways in a highly cell-type-specific manner, underscoring the role of functional reconfiguration of conserved circuits in behavioral evolution. Further investigation of sex differences in + neurons revealed that male-specific cell types are not more evolutionarily divergent than sex-unbiased ones. Finally, we developed an interactive web resource for data access and characterized marker gene combinations enabling cell-type-specific labeling. Overall, our study provides insights into how neural circuits evolve to encode behavioral diversity and establishes a high-resolution framework for understanding the cellular basis of behavioral adaptation.
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ISSN:1091-6490
1091-6490
DOI:10.1073/pnas.2516083122