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Open Access Research article

Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus)

Amy L Toth12*, John F Tooker3, Srihari Radhakrishnan1, Robert Minard4, Michael T Henshaw5 and Christina M Grozinger3

Author Affiliations

1 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA

2 Department of Entomology, Iowa State University, Ames, IA, USA

3 Department of Entomology, Center for Pollinator Research, Center for Chemical Ecology, The Pennsylvania State University, University Park, PA, USA

4 Proteomics and Mass Spectrometry Core Facility, Huck Institutes for the Life Sciences, The Pennsylvania State University, University Park, PA, USA

5 Department of Biology, Grand Valley State University, Allendale, MI, USA

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BMC Genomics 2014, 15:75  doi:10.1186/1471-2164-15-75

Published: 28 January 2014

Abstract

Background

In social groups, dominant individuals may socially inhibit reproduction of subordinates using aggressive interactions or, in the case of highly eusocial insects, pheromonal communication. It has been hypothesized these two modes of reproductive inhibition utilize conserved pathways. Here, we use a comparative framework to investigate the chemical and genomic underpinnings of reproductive dominance in the primitively eusocial wasp Polistes metricus. Our goals were to first characterize transcriptomic and chemical correlates of reproductive dominance and second, to test whether dominance-associated mechanisms in paper wasps overlapped with aggression or pheromone-related gene expression patterns in other species. To explore whether conserved molecular pathways relate to dominance, we compared wasp transcriptomic data to previous studies of gene expression associated with pheromonal communication and queen-worker differences in honey bees, and aggressive behavior in bees, Drosophila, and mice.

Results

By examining dominant and subordinate females from queen and worker castes in early and late season colonies, we found that cuticular hydrocarbon profiles and genome-wide patterns of brain gene expression were primarily associated with season/social environment rather than dominance status. In contrast, gene expression patterns in the ovaries were associated primarily with caste and ovary activation. Comparative analyses suggest genes identified as differentially expressed in wasp brains are not related to queen pheromonal communication or caste in bees, but were significantly more likely to be associated with aggression in other insects (bees, flies), and even a mammal (mice).

Conclusions

This study provides the first comprehensive chemical and molecular analysis of reproductive dominance in paper wasps. We found little evidence for a chemical basis for reproductive dominance in P. metricus, and our transcriptomic analyses suggest that different pathways regulate dominance in paper wasps and pheromone response in bees. Furthermore, there was a substantial impact of season/social environment on gene expression patterns, indicating the important role of external cues in shaping the molecular processes regulating behavior. Interestingly, genes associated with dominance in wasps were also associated with aggressive behavior in bees, solitary insects and mammals. Thus, genes involved in social regulation of reproduction in Polistes may have conserved functions associated with aggression in insects and other taxa.

Keywords:
Wasps; Social behavior; Genomics; Aggression; Pheromones; Chemical communication