Submitted to: PLoS Genetics
Publication Type: Peer reviewed journal
Publication Acceptance Date: 5/30/2013
Publication Date: 8/8/2013
Citation: Manfredini, F., Riba-Grognuz, O., Wurm, Y., Keller, L., Shoemaker, D.D., Grozinger, C.M. 2013. Sociogenomics of cooperation and conflict during colony foundation in the fire ant Solenopsis invicta. PLoS Genetics. 9(8): 1-15. Interpretive Summary: Fire ants are considered significant ecological, agricultural, and public health pest throughout their invasive range in the U.S.A. A research entomologist at the Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, Gainesville, Florida, in collaboration with scientists from the University of Lausanne and Pennsylvania State University describe here the results of a study using newly developed whole-genome microarrays to characterize the gene expression patterns underpinning different behavioral phenotypes of foundress fire ant queens. The results demonstrate that in the fire ant S. invicta, social environment (colonies started by single-queen vs. multiple-queens) plays a major role in the determination of the patterns of gene expression, while the physiological state and the social rank of founding queens are only secondary. These results highlight the powerful influence of social environment on regulation of gene expression patterns, physiology and, ultimately, social behavior of animals.
Technical Abstract: The genomic state of an individual results from the interplay between its internal condition and the external environment, which may include the social environment. The link between genes and social environment is clearly visible during the process of colony founding in the fire ant Solenopsis invicta. This is a complex process that can be used as a model to investigate how the interplay between genes and social environment has shaped the evolution of social behavior. Newly-mated queens of the monogyne (single queen per colony) social form are very similar anatomically and physiologically but may adopt two drastically different strategies to start a new colony: they can do so 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 during queen-queen fights or by workers. In this study we used newly developed whole-genome microarrays to characterize the gene expression patterns underpinning these different behavioral phenotypes. First, we compared haplometrotic queens and pleometrotic winners and losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social rank of the two cofoundresses: putative winners (or losers) were paired with new partners such that they became losers (or winners), or maintained the same social rank. A large set of transcripts were significantly differentially regulated between haplometrotic and pleometrotic queens. Overrepresented biological categories included basic functions such as metabolism, development, cell organization and biogenesis, but also more specific processes such as stress response, aging, immunity, reproduction and lipid biosynthesis. Expression differences for several candidate genes involved in these biological processes were confirmed using quantitative real-time PCR. Only a few transcripts were significantly differentially regulated between winners and losers in pleometrotic associations: these transcripts were mainly associated with the metabolism of fatty acids and hormones. Similarly, only a small set of transcripts was significantly differentially regulated after social rank manipulation, including those involved in lipid biosynthesis and response to stress. Our findings indicate that in the fire ant S. invicta, social environment (haplometrosis vs. pleometrosis) plays a major role in the determination of the patterns of gene expression, while the physiological state and the social rank of founding queens are only secondary. These results highlight the powerful influence of social environment on regulation of gene expression patterns, physiology and, ultimately, social behavior of animals.