Drosulfakinin signaling encodes early-life memory for adaptive social plasticity
- Ulsan National Institute of Science and Technology, Republic of Korea
- Korea Advanced Institute of Science and Technology, Republic of Korea
Abstract
Drosophila establishes social clusters in groups, yet the underlying principles remain poorly understood. Here we performed a systemic analysis of social network behavior (SNB) that quantifies individual social distance (SD) in a group over time. The SNB assessment in 175 inbred strains from the Drosophila Genetics Reference Panel showed a tight association of short SD with long developmental time, low food intake, and hypoactivity. The developmental inferiority in short-SD individuals was compensated by their group culturing. By contrast, developmental isolation silenced the beneficial effects of social interactions in adults and blunted the plasticity of SNB under physiological challenges. Transcriptome analyses revealed genetic diversity for SD traits, whereas social isolation reprogrammed select genetic pathways, regardless of SD phenotypes. In particular, social deprivation suppressed the expression of the neuropeptide Drosulfakinin (Dsk) in three pairs of adult brain neurons. Male-specific DSK signaling to Cholecystokinin-like receptor 17D1 mediated the SNB plasticity. In fact, transgenic manipulations of the DSK neuron activity were sufficient to imitate the state of social experience. Given the functional conservation of mammalian Dsk homologs, we propose that animals may have evolved a dedicated neural mechanism to encode early-life experience and transform group properties adaptively.
Data availability
The datasets generated and analyzed during the current study are included in Dataset S6 or available in the European Nucleotide Archive repository (accession number PRJEB61423). The python scripts that support the findings of this study are available from the author's GitHub webpage under the links https://github.com/jiunbae/tracking-fly and https://github.com/KJKwon/2023_FlyBehavior.
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Author details
Funding
Suh Kyungbae Foundation (SUHF-17020101)
- Chunghun Lim
National Research Foundation of Korea (NRF-2021M3A9G8022960)
- Chunghun Lim
National Research Foundation of Korea (NRF-2018R1A5A1024261)
- Chunghun Lim
National Research Foundation of Korea (NRF-2023R1A2C100627511)
- Taejoon Kwon
National Research Foundation of Korea (NRF-2018R1A6A1A03025810)
- Taejoon Kwon
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2024, Jeong et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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Drosulfakinin signaling encodes early-life memory for adaptive social plasticity
eLife 13:e103973.
https://doi.org/10.7554/eLife.103973
