IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40331-9.html
   My bibliography  Save this article

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

Author

Listed:
  • Zachary V. Johnson

    (Georgia Institute of Technology
    Georgia Institute of Technology
    Emory University
    Emory University)

  • Brianna E. Hegarty

    (Georgia Institute of Technology
    Georgia Institute of Technology)

  • George W. Gruenhagen

    (Georgia Institute of Technology
    Georgia Institute of Technology)

  • Tucker J. Lancaster

    (Georgia Institute of Technology
    Georgia Institute of Technology)

  • Patrick T. McGrath

    (Georgia Institute of Technology
    Georgia Institute of Technology)

  • Jeffrey T. Streelman

    (Georgia Institute of Technology
    Georgia Institute of Technology)

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.

Suggested Citation

  • Zachary V. Johnson & Brianna E. Hegarty & George W. Gruenhagen & Tucker J. Lancaster & Patrick T. McGrath & Jeffrey T. Streelman, 2023. "Cellular profiling of a recently-evolved social behavior in cichlid fishes," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40331-9
    DOI: 10.1038/s41467-023-40331-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40331-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40331-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Hyejung Won & Jerry Huang & Carli K. Opland & Chris L. Hartl & Daniel H. Geschwind, 2019. "Human evolved regulatory elements modulate genes involved in cortical expansion and neurodevelopmental disease susceptibility," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    3. Benjamin Lacar & Sara B. Linker & Baptiste N. Jaeger & Suguna Rani Krishnaswami & Jerika J. Barron & Martijn J. E. Kelder & Sarah L. Parylak & Apuã C. M. Paquola & Pratap Venepally & Mark Novotny & Ca, 2016. "Nuclear RNA-seq of single neurons reveals molecular signatures of activation," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    4. Elizabeth A. Amadei & Zachary V. Johnson & Yong Jun Kwon & Aaron C. Shpiner & Varun Saravanan & Wittney D. Mays & Steven J. Ryan & Hasse Walum & Donald G. Rainnie & Larry J. Young & Robert C. Liu, 2017. "Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles," Nature, Nature, vol. 546(7657), pages 297-301, June.
    5. Daniel Dimitrov & Dénes Türei & Martin Garrido-Rodriguez & Paul L. Burmedi & James S. Nagai & Charlotte Boys & Ricardo O. Ramirez Flores & Hyojin Kim & Bence Szalai & Ivan G. Costa & Alberto Valdeoliv, 2022. "Comparison of methods and resources for cell-cell communication inference from single-cell RNA-Seq data," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Johannes Kohl & Benedicte M. Babayan & Nimrod D. Rubinstein & Anita E. Autry & Brenda Marin-Rodriguez & Vikrant Kapoor & Kazunari Miyamishi & Larry S. Zweifel & Liqun Luo & Naoshige Uchida & Catherine, 2018. "Functional circuit architecture underlying parental behaviour," Nature, Nature, vol. 556(7701), pages 326-331, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. JANSSENS, Jochen & DE CORTE, Annelies & SÖRENSEN, Kenneth, 2016. "Water distribution network design optimisation with respect to reliability," Working Papers 2016007, University of Antwerp, Faculty of Business and Economics.
    2. Raymond Hernandez & Elizabeth A. Pyatak & Cheryl L. P. Vigen & Haomiao Jin & Stefan Schneider & Donna Spruijt-Metz & Shawn C. Roll, 2021. "Understanding Worker Well-Being Relative to High-Workload and Recovery Activities across a Whole Day: Pilot Testing an Ecological Momentary Assessment Technique," IJERPH, MDPI, vol. 18(19), pages 1-17, October.
    3. Elisabeth Beckmann & Lukas Olbrich & Joseph Sakshaug, 2024. "Multivariate assessment of interviewer-related errors in a cross-national economic survey (Lukas Olbrich, Elisabeth Beckmann, Joseph W. Sakshaug)," Working Papers 253, Oesterreichische Nationalbank (Austrian Central Bank).
    4. Valentina Krenz & Arjen Alink & Tobias Sommer & Benno Roozendaal & Lars Schwabe, 2023. "Time-dependent memory transformation in hippocampus and neocortex is semantic in nature," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Morán-Ordóñez, Alejandra & Ameztegui, Aitor & De Cáceres, Miquel & de-Miguel, Sergio & Lefèvre, François & Brotons, Lluís & Coll, Lluís, 2020. "Future trade-offs and synergies among ecosystem services in Mediterranean forests under global change scenarios," Ecosystem Services, Elsevier, vol. 45(C).
    6. Damian M. Herz & Manuel Bange & Gabriel Gonzalez-Escamilla & Miriam Auer & Keyoumars Ashkan & Petra Fischer & Huiling Tan & Rafal Bogacz & Muthuraman Muthuraman & Sergiu Groppa & Peter Brown, 2022. "Dynamic control of decision and movement speed in the human basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Dongyan Liu & Chongran Zhou & John K. Keesing & Oscar Serrano & Axel Werner & Yin Fang & Yingjun Chen & Pere Masque & Janine Kinloch & Aleksey Sadekov & Yan Du, 2022. "Wildfires enhance phytoplankton production in tropical oceans," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    8. Zhaogeng Yang & Yanhui Li & Peijin Hu & Jun Ma & Yi Song, 2020. "Prevalence of Anemia and its Associated Factors among Chinese 9-, 12-, and 14-Year-Old Children: Results from 2014 Chinese National Survey on Students Constitution and Health," IJERPH, MDPI, vol. 17(5), pages 1-10, February.
    9. Marco Lopez-Cruz & Fernando M. Aguate & Jacob D. Washburn & Natalia Leon & Shawn M. Kaeppler & Dayane Cristina Lima & Ruijuan Tan & Addie Thompson & Laurence Willard Bretonne & Gustavo los Campos, 2023. "Leveraging data from the Genomes-to-Fields Initiative to investigate genotype-by-environment interactions in maize in North America," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    10. Baumann, Elias & Kern, Jana & Lessmann, Stefan, 2019. "Usage Continuance in Software-as-a-Service," IRTG 1792 Discussion Papers 2019-005, Humboldt University of Berlin, International Research Training Group 1792 "High Dimensional Nonstationary Time Series".
    11. repec:cup:judgdm:v:16:y:2021:i:1:p:201-237 is not listed on IDEAS
    12. C. Gabriel Hidalgo Pizango & Eurídice N. Honorio Coronado & Jhon del Águila-Pasquel & Gerardo Flores Llampazo & Johan de Jong & César J. Córdova Oroche & José M. Reyna Huaymacari & Steve J. Carver & D, 2022. "Sustainable palm fruit harvesting as a pathway to conserve Amazon peatland forests," Nature Sustainability, Nature, vol. 5(6), pages 479-487, June.
    13. Szefer Elena & Graham Jinko & Lu Donghuan & Beg Mirza Faisal & Nathoo Farouk, 2017. "Multivariate association between single-nucleotide polymorphisms in Alzgene linkage regions and structural changes in the brain: discovery, refinement and validation," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 16(5-6), pages 349-365, December.
    14. Julien Collet & Samantha C Patrick & Henri Weimerskirch, 2017. "A comparative analysis of the behavioral response to fishing boats in two albatross species," Behavioral Ecology, International Society for Behavioral Ecology, vol. 28(5), pages 1337-1347.
    15. Sean Coogan & Zhixian Sui & David Raubenheimer, 2018. "Gluttony and guilt: monthly trends in internet search query data are comparable with national-level energy intake and dieting behavior," Palgrave Communications, Palgrave Macmillan, vol. 4(1), pages 1-9, December.
    16. Darcy Steeg Morris & Kimberly F. Sellers, 2022. "A Flexible Mixed Model for Clustered Count Data," Stats, MDPI, vol. 5(1), pages 1-18, January.
    17. Katrijn Delaruelle, 2023. "Migration-related inequalities in loneliness across age groups: a cross-national comparative study in Europe," European Journal of Ageing, Springer, vol. 20(1), pages 1-17, December.
    18. Christos C Ioannou & Luis Arrochela Braga Carvalho & Chessy Budleigh & Graeme D Ruxton, 2023. "Virtual prey with Lévy motion are preferentially attacked by predatory fish," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(4), pages 695-699.
    19. Vonneilich, Nico & Lüdecke, Daniel & von dem Knesebeck, Olaf, 2020. "Educational inequalities in self-rated health and social relationships – analyses based on the European Social Survey 2002-2016," Social Science & Medicine, Elsevier, vol. 267(C).
    20. Kimmo Eriksson & Irina Vartanova & Petra Ornstein & Pontus Strimling, 2021. "The common-is-moral association is stronger among less religious people," Palgrave Communications, Palgrave Macmillan, vol. 8(1), pages 1-8, December.
    21. Sarah V Bentley & Katharine H Greenaway & S Alexander Haslam, 2017. "An online paradigm for exploring the self-reference effect," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-21, May.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40331-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.