Drosulfakinin signaling encodes early-life memory for adaptive social plasticity
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 Dr...
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eLife Sciences Publications Ltd
2024-12-01
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| Online Access: | https://elifesciences.org/articles/103973 |
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| author | Jiwon Jeong Kujin Kwon Terezia Klaudia Geisseova Jongbin Lee Taejoon Kwon Chunghun Lim |
| author_facet | Jiwon Jeong Kujin Kwon Terezia Klaudia Geisseova Jongbin Lee Taejoon Kwon Chunghun Lim |
| author_sort | Jiwon Jeong |
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| description | 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. |
| format | Article |
| id | doaj-art-23591039339047e0a2c2ecefa2f01b15 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2024-12-01 |
| publisher | eLife Sciences Publications Ltd |
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| spelling | doaj-art-23591039339047e0a2c2ecefa2f01b152025-01-07T15:24:58ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.103973Drosulfakinin signaling encodes early-life memory for adaptive social plasticityJiwon Jeong0https://orcid.org/0009-0006-3111-2656Kujin Kwon1https://orcid.org/0009-0004-6642-222XTerezia Klaudia Geisseova2Jongbin Lee3https://orcid.org/0000-0002-5868-7437Taejoon Kwon4https://orcid.org/0000-0002-9794-6112Chunghun Lim5https://orcid.org/0000-0001-8473-9272Department of Biological Sciences, Ulsan National Institute of Science and Technology, Ulsan, Republic of KoreaDepartment of Biomedical Engineering, Ulsan National Institute of Science and Technology, Ulsan, Republic of KoreaDepartment of Biological Sciences, Ulsan National Institute of Science and Technology, Ulsan, Republic of KoreaResearch Center for Cellular Identity, Korea Advanced Institute of Science and Technology, Daejeon, Republic of KoreaDepartment of Biomedical Engineering, Ulsan National Institute of Science and Technology, Ulsan, Republic of Korea; Center for Genomic Integrity, Institute for Basic Science, Ulsan, Republic of Korea; Graduate School of Health Science and Technology, Ulsan National Institute of Science and Technology, Ulsan, Republic of KoreaResearch Center for Cellular Identity, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea; Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea; Graduate School of Stem Cell and Regenerative Biology, Korea Advanced Institute of Science and Technology, Daejeon, Republic of KoreaDrosophila 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.https://elifesciences.org/articles/103973Drosophilasocial network behaviorearly-life experiencesocial memoryDrosulfakinin |
| spellingShingle | Jiwon Jeong Kujin Kwon Terezia Klaudia Geisseova Jongbin Lee Taejoon Kwon Chunghun Lim Drosulfakinin signaling encodes early-life memory for adaptive social plasticity eLife Drosophila social network behavior early-life experience social memory Drosulfakinin |
| title | Drosulfakinin signaling encodes early-life memory for adaptive social plasticity |
| title_full | Drosulfakinin signaling encodes early-life memory for adaptive social plasticity |
| title_fullStr | Drosulfakinin signaling encodes early-life memory for adaptive social plasticity |
| title_full_unstemmed | Drosulfakinin signaling encodes early-life memory for adaptive social plasticity |
| title_short | Drosulfakinin signaling encodes early-life memory for adaptive social plasticity |
| title_sort | drosulfakinin signaling encodes early life memory for adaptive social plasticity |
| topic | Drosophila social network behavior early-life experience social memory Drosulfakinin |
| url | https://elifesciences.org/articles/103973 |
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