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Genome Biol Evol. 2017 Nov 1;9(11):3059-3072. doi: 10.1093/gbe/evx220.

Neurogenomic Signatures of Successes and Failures in Life-History Transitions in a Key Insect Pollinator.

Author information

1
School of Biological Sciences, Royal Holloway University of London, Egham, United Kingdom.
2
Department of Computer Science, and Centre for Systems and Synthetic Biology, Royal Holloway University of London, Egham, United Kingdom.
3
Center for Systems Biotechnology, Fraunhofer Chile Research Foundation, Santiago, Chile.
4
School of Biological Sciences, University of Bristol, United Kingdom.
5
Centre for Biodiversity & Environment Research, Department of Genetics, Evolution & Environment, University College London, London, United Kingdom.

Abstract

Life-history transitions require major reprogramming at the behavioral and physiological level. Mating and reproductive maturation are known to trigger changes in gene transcription in reproductive tissues in a wide range of organisms, but we understand little about the molecular consequences of a failure to mate or become reproductively mature, and it is not clear to what extent these processes trigger neural as well as physiological changes. In this study, we examined the molecular processes underpinning the behavioral changes that accompany the major life-history transitions in a key pollinator, the bumblebee Bombus terrestris. We compared neuro-transcription in queens that succeeded or failed in switching from virgin and immature states, to mated and reproductively mature states. Both successes and failures were associated with distinct molecular profiles, illustrating how development during adulthood triggers distinct molecular profiles within a single caste of a eusocial insect. Failures in both mating and reproductive maturation were explained by a general up-regulation of brain gene transcription. We identified 21 genes that were highly connected in a gene coexpression network analysis: nine genes are involved in neural processes and four are regulators of gene expression. This suggests that negotiating life-history transitions involves significant neural processing and reprogramming, and not just changes in physiology. These findings provide novel insights into basic life-history transitions of an insect. Failure to mate or to become reproductively mature is an overlooked component of variation in natural systems, despite its prevalence in many sexually reproducing organisms, and deserves deeper investigation in the future.

KEYWORDS:

Bombus terrestris; brain; bumblebee; gene network; mating; reproductive maturation

PMID:
29087523
PMCID:
PMC5714134
DOI:
10.1093/gbe/evx220
[Indexed for MEDLINE]
Free PMC Article

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