Social Isolation and Group Size are Associated with Divergent Gene Expression in the Brain of Ant Queens

Fabio Manfredini* (Corresponding Author), Carlos Martinez-Ruiz , Yannick Wurm, Dewayne Shoemaker, Mark Brown

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)
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Abstract

Social life and isolation pose a complex suite of challenges to organisms prompting significant changes in neural state. However, plasticity in how brains respond to social challenges remains largely unexplored. The fire ants Solenopsis invicta provide an ideal scenario for examining this. Fire ant queens may found colonies individually or in groups of up to 30 queens, depending on key factors such as density of newly mated queens and availability of nesting sites. We artificially manipulated availability of nesting sites to test how the brain responds to social vs. solitary colony founding at two key timepoints (early vs. late colony founding) and to group size (large vs. small groups). We adopted a powerful neurogenomic approach to identify even subtle differences of gene expression between treatment groups, and we built a global gene co-expression network of the fire ant brain to identify gene modules specifically associated with the different components of the social environment. The difference between group and single founding queens involves only 1 gene when founding behaviour is still plastic and queens can switch from one modality to another, while hundreds of genes are involved later in the process, when behaviours have lost the initial plasticity and are more canalized. Furthermore, we find that large groups are associated with greater changes in gene expression than small groups, showing that even potentially subtle differences in the social environment can be linked to different neurogenomic states.
Original languageEnglish
Article numbere12758
Number of pages12
JournalGenes, Brain, and Behavior
Volume21
Issue number3
Early online date20 Jun 2021
DOIs
Publication statusPublished - 1 Mar 2022

Bibliographical note

ACKNOWLEDGEMENTS
The authors would like to thank members of the Shoemaker’s Lab at the USDA-ARS in Gainesville for support during field experiments and sample collections: special thanks to Eileen Carroll who coordinated all activities associated with field experiments and arranged the shipment of samples to the UK. The authors would also like to thank all members of the Leadbeater Lab at Royal Holloway for providing feedback on an early draft of this manuscript, and the two anonymous reviewers who provided constructive criticism that helped improving the manuscript. This work was supported by a Marie Curie International Incoming Fellowship (FP7-PEOPLE-2013-IIF-625487) to F.M. and M.J.F.B. which also supported F.M. salary for two years. The Natural Environment Research Council supported the salaries of C.M.R. (NE/L002485/1) and Y.W. (NE/L00626X/1). The authors declare that they have no conflict of interest.

Open access via Wiley agreement

Data Availability Statement

RNAseq data that support the findings of this study have been depos- ited in NCBI BioProject Submissions with the SubmissionID: SUB5134076s and BioProject ID: PRJNA525584 (www.ncbi.nlm.nih. gov/bioproject/?term=PRJNA525584). All codes used for the analyses described in the manuscript are publicly available on GitHub (github.com/FabioManfre/Solenopsis_RNAseq_founding-queens).

Keywords

  • colony founding
  • fire ants
  • gene expression
  • group size
  • isolation
  • social behaviour
  • Solenopsis invicta

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