Neurogenomic  signatures of successes and failures in core life-history transitions in a key insect pollinator

The switch between biological states during key life-history transitions requires major reprogramming at the behavioural level that is under the control of the brain. In this study we focused on major life-history transitions in bumblebee queens (Bombus terrestris) that involve switching from virgin to mated and reproductively mature. To reveal the molecular processes underpinning the behavioural changes that accompany these transitions, we characterised the neurogenomic state of queens that succeeded or failed in making these transitions. Analyses of shared transcription patterns suggested that failures are associated with larger molecular signatures than successes. This was observed at the level of total numbers of differentially expressed genes (DEGs) and proportions of these genes that were up-regulated, and applies to both mating and reproductive maturation. 'Failed Reproductive' queens were the most distinct phenotype, associated with the highest number of DEGs (1,578) and two networks of co-expressed genes. Mating status influenced gene expression the least, followed by the transition between the two successful phenotypes (mating to reproductive maturation) and reproductive maturation. However, this pattern was not mirrored in terms of functional specialisations, for Gene Ontology (GO) terms, KEGG pathways and co-expression networks associated with DEGs. Out of the 21 highly connected (hub) genes associated with co-expression networks, 9 are involved in neural processes and 4 are regulators of gene expression. This study shows that different life-history transitions trigger distinct molecular profiles, within a single caste of a eusocial insect. Failure to surmount key life-history transitions has the largest effect on a queen's neurogenomic state, and it triggers a massive overall up-regulation of gene expression. Hence, failure is an important outcome that must be taken into account when analysing the molecular regulation of important life-history transitions. Overall design: Brain RNA samples for 4 treatments: successfully mated (SM, N=8), failed mated (failed mated, N=9), successfully reproductive (SR, N=8) and failed reproductive (FR, N=8)

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