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

Abstract

BackgroundUnderstanding 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.ResultscDNA 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.ConclusionsDetailed 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.

Gene Expression Dynamics in Major Endocrine Regulatory Pathways along the Transition from Solitary to Social Life in a Bumblebee, Bombus terrestris

“…In bumblebees, the presence of queen diapause has been proposed to be a prerequisite for the evolution of sociality by co-option of the diapause-regulating gene network for new roles in caste differentiation (Hunt and Amdam, 2005; Hunt et al, 2007). Several studies have investigated the genetics underlying diapause in bumblebees (Kim et al, 2006, 2008; Colgan et al, 2011), including a very recent study communicating a genome-wide transcriptome comparison targeting the fat body of diapausing Bombus terrestris queens (Amsalem et al, 2015b). The latter study, concurrent with our own investigations, highlighted the functional association of the genes highly expressed in the queen's fat body with nutrient storage and stress resistance, as well as a different role of JH and Vg in diapausing bumblebee queens when compared to dipteran models.…”

RNA-Seq reveals that mitochondrial genes and long non-coding RNAs may play important roles in the bivoltine generations of the non-social Neotropical bee Tetrapedia diversipes

“…Quality analyses of the transcripts indicate that the assembly is comparable to other bee transcriptomes (Colgan et al 2011;Kocher et al 2013;Rehan et al 2014;Harrison et al 2015) and has a high sequencing coverage (about 150 x per transcriptome). In both life cycle stages, more than 60% (60.9% in adult females and 66.2% in larvae) of the transcripts had a significant blast hit against a sequence in the UniRef database, especially against bees and other Hymenoptera sequences (Online Resource 3).…”

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

“…Functional genomic techniques, such as RNA‐Seq, provide an unbiased view into genome‐wide transcriptional changes and have been applied to microparasite–insect systems to elucidate genes underlying complex altered host phenotypes (Choi et al ., ; Geffre et al ., ). For the bumblebee, recent developments in genomics and transcriptomics have provided the tools to explore important aspects of host biology, including phenotypic polymorphism (Colgan et al ., ; Harrison et al ., ), caste differentiation (Collins et al ., ; Woodard et al ., ), mating success (Manfredini et al ., ) and diapause regulation (Amsalem et al ., ). In relation to pathogen response, previous transcriptomic studies have identified changes in host immune expression in response to the trypanosomatid Crithidia bombi (Barribeau et al ., ) and bacterial challenge (Barribeau et al ., ).…”