Early Life Experience Shapes Male Behavior and Social Networks in Drosophila

Assa Bentzur, Shir Ben-Shaanan, Jennifer I.C. Benichou, Eliezer Costi, Amiyaal Ilany, Galit Shohat-Ophir

Research output: Contribution to journalArticlepeer-review

13 Scopus citations

Abstract

Living in a group creates a complex and dynamic environment in which behavior of individuals is influenced by and affects the behavior of others. Although social interaction and group living are fundamental adaptations exhibited by many organisms, little is known about how prior social experience, internal states, and group composition shape behavior in groups. Here, we present an analytical framework for studying the interplay between social experience and group interaction in Drosophila melanogaster. We simplified the complexity of interactions in a group using a series of experiments in which we controlled the social experience and motivational states of individuals to compare behavioral patterns and social networks of groups under different conditions. We show that social enrichment promotes the formation of distinct group structure that is characterized by high network modularity, high inter-individual and inter-group variance, high inter-individual coordination, and stable social clusters. Using environmental and genetic manipulations, we show that visual cues and cVA-sensing neurons are necessary for the expression of social interaction and network structure in groups. Finally, we explored the formation of group behavior and structure in heterogenous groups composed of flies with distinct internal states and documented emergent structures that are beyond the sum of the individuals that constitute it. Our results demonstrate that fruit flies exhibit complex and dynamic social structures that are modulated by the experience and composition of different individuals within the group. This paves the path for using simple model organisms to dissect the neurobiology of behavior in complex social environments.

Original languageEnglish
Pages (from-to)486-501.e3
JournalCurrent Biology
Volume31
Issue number3
DOIs
StatePublished - 8 Feb 2021

Bibliographical note

Funding Information:
We thank all members of the Shohat-Ophir and Ilany labs for fruitful discussions and technical support. We specially thank Kristin Branson and Alice Robie (HHMI Janelia research campus) for their valuable advice and guidance with the experimental and computational design and Karla Kaun (Brown University) for her productive suggestions. We specially thank Moshe Ben Shaanan for his mentorship and support in FixTRAX design. This work was supported by the Israel Science Foundation grant 384/14 , Israel Science Foundation grant 174/19 , and Israel Science Foundation grant 244/19 .

Publisher Copyright:
© 2020 Elsevier Inc.

Keywords

  • Drosophila melanogaster
  • group
  • internal state
  • motivation
  • social experience
  • social interaction
  • social networks

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