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Open Access Research article

Polyphenism in social insects: insights from a transcriptome-wide analysis of gene expression in the life stages of the key pollinator, Bombus terrestris

Thomas J Colgan1*, James C Carolan12, Stephen J Bridgett3, Seirian Sumner4, Mark L Blaxter35 and Mark JF Brown16

Author Affiliations

1 Department of Zoology, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland

2 Department of Biology, Callan Building, National University of Ireland Maynooth, Maynooth, Co. Kildare, Ireland

3 The GenePool Genomics Facility, School of Biological Sciences, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK

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

5 Institute of Evolutionary Biology, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK

6 School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey, TW20 0EX, UK

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BMC Genomics 2011, 12:623  doi:10.1186/1471-2164-12-623

Published: 20 December 2011

Abstract

Background

Understanding polyphenism, the ability of a single genome to express multiple morphologically and behaviourally distinct phenotypes, is an important goal for evolutionary and developmental biology. Polyphenism has been key to the evolution of the Hymenoptera, and particularly the social Hymenoptera where the genome of a single species regulates distinct larval stages, sexual dimorphism and physical castes within the female sex. Transcriptomic analyses of social Hymenoptera will therefore provide unique insights into how changes in gene expression underlie such complexity. Here we describe gene expression in individual specimens of the pre-adult stages, sexes and castes of the key pollinator, the buff-tailed bumblebee Bombus terrestris.

Results

cDNA was prepared from mRNA from five life cycle stages (one larva, one pupa, one male, one gyne and two workers) and a total of 1,610,742 expressed sequence tags (ESTs) were generated using Roche 454 technology, substantially increasing the sequence data available for this important species. Overlapping ESTs were assembled into 36,354 B. terrestris putative transcripts, and functionally annotated. A preliminary assessment of differences in gene expression across non-replicated specimens from the pre-adult stages, castes and sexes was performed using R-STAT analysis. Individual samples from the life cycle stages of the bumblebee differed in the expression of a wide array of genes, including genes involved in amino acid storage, metabolism, immunity and olfaction.

Conclusions

Detailed analyses of immune and olfaction gene expression across phenotypes demonstrated how transcriptomic analyses can inform our understanding of processes central to the biology of B. terrestris and the social Hymenoptera in general. For example, examination of immunity-related genes identified high conservation of important immunity pathway components across individual specimens from the life cycle stages while olfactory-related genes exhibited differential expression with a wider repertoire of gene expression within adults, especially sexuals, in comparison to immature stages. As there is an absence of replication across the samples, the results of this study are preliminary but provide a number of candidate genes which may be related to distinct phenotypic stage expression. This comprehensive transcriptome catalogue will provide an important gene discovery resource for directed programmes in ecology, evolution and conservation of a key pollinator.