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Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes

Pedro G Ferreira16, Solenn Patalano23, Ritika Chauhan4, Richard Ffrench-Constant4, Toni Gabaldón1, Roderic Guigó1 and Seirian Sumner25*

Author affiliations

1 Center for Genomic Regulation, Universitat Pompeu Fabra (CRG-UPF), Doctor Aiguader, 88, 08003 Barcelona, Catalonia, Spain

2 Institute of Zoology, Zoological Society of London, Regent's Park, NW1 4RY, UK

3 The Babraham Institute, Babraham Research Campus, Cambridge, CB22 3AT, UK

4 Centre for Ecology and Conservation, Biosciences, University of Exeter, Tremough, Penryn, TR10 9EZ, UK

5 Current address: School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK

6 Current address: Department of Genetic Medicine and Development, University of Geneva Medical School, 25 Rue Michel Servet 1, 1211 Geneva, Switzerland

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Citation and License

Genome Biology 2013, 14:R20  doi:10.1186/gb-2013-14-2-r20

Published: 26 February 2013

Abstract

Background

Understanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution.

Results

We sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways.

Conclusions

These genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.