Sociogenomics of conflict and cooperation during colony founding in the fire ant Solenopsis invicta

Fabio Manfredini*, Oksana Riba-Grognuz, Yannick Wurm, Laurent Keller, DeWayne Shoemaker, Christina Grozinger

*Corresponding author for this work

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29 Citations (Scopus)
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One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the “winner”) in pleometrotic associations survives and takes the lead of the young colony while the others (the “losers”) are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.
Original languageEnglish
Article numbere1003633
Number of pages15
JournalPLoS Genetics
Issue number8
Early online date8 Aug 2013
Publication statusPublished - Aug 2013

Bibliographical note

The authors would like to thank members of the Grozinger Lab for commenting on an earlier version of the manuscript and Sarah Kocher (Harvard) and Naomi Altman (Penn State) for providing assistance with the statistical analysis. The authors would also like to thank Alex McMenamin for performing the validation of candidate gene expression. Many thanks to Craig Praul and his team at the Penn State Genomics Core Facility for performing all the steps to prepare RNA samples for microarrays and for providing assistance during RNA extraction and data analysis. A special thanks to Eileen Carroll, Chin-Cheng Yang (Scotty) and all the undergraduate research assistants in the Shoemaker Lab that provided extraordinary support, help and advice during field work and laboratory experiments at the USDA-ARS, CMAVE in Gainesville, Florida.

Funding: This study was funded by US Department of Agriculture AFRI Award 2009-35302-05301 to DS and CMG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.


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