Cellular profiling of a recently-evolved social behavior in cichlid fishes

• Type of Material: Article
• Authors: Zachary Johnson, Emory University; Brianna E. Hegarty, Georgia Institute of Technology; George W. Gruenhagen, Georgia Institute of Technology; Tucker J. Lancaster, Georgia Institute of Technology; Patrick T. McGrath, Georgia Institute of Technology; Jeffrey T. Streelman, Georgia Institute of Technology
• Language: English
• Date: 2023-12-01
• Publisher: Nature
• Publication Version: Final Published Version
• Copyright Statement: © The Author(s) 2023
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1038/s41467-023-40331-9
• Title of Journal or Parent Work: Nature Communications
• Volume: 14
• Issue: 1
• Start Page: 4891
• End Page: 4891
• Grant/Funding Information: This work was supported in part by NIH R01GM101095 and R01GM144560 to J.T.S., NIH F32GM128346 to Z.V.J., NIH R35 GM139594 to P.T.M., NSF Graduate Research Fellowship DGE-2039655 to T.J.L., and Human Frontiers Science Program RGP0052/2019 to J.T.S.
• Keywords: Genomics; Genome; Animals; Cichlids; Base Sequence; Social Behavior
• Research Categories: Biology, Genetics; Biology, Animal Physiology

Abstract

Social behaviors are diverse in nature, but it is unclear how conserved genes, brain regions, and cell populations generate this diversity. Here we investigate bower-building, a recently-evolved social behavior in cichlid fishes. We use single nucleus RNA-sequencing in 38 individuals to show signatures of recent behavior in specific neuronal populations, and building-associated rebalancing of neuronal proportions in the putative homolog of the hippocampal formation. Using comparative genomics across 27 species, we trace bower-associated genome evolution to a subpopulation of glia lining the dorsal telencephalon. We show evidence that building-associated neural activity and a departure from quiescence in this glial subpopulation together regulate hippocampal-like neuronal rebalancing. Our work links behavior-associated genomic variation to specific brain cell types and their functions, and suggests a social behavior has evolved through changes in glia.