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

Fabio Manfredini* (Corresponding Author), Alfonso E Romero , Inti Pedroso , Alberto Paccanaro, Seirian Sumner, Mark J F Brown

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

14 Citations (Scopus)
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Life-history transitions require major reprogramming at the behavioural 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 behavioural 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 co-expression network analysis: 9 genes are involved in neural processes and 4 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.
Original languageEnglish
Pages (from-to)3059-3072
Number of pages14
JournalGenome biology and evolution
Issue number11
Early online date26 Oct 2017
Publication statusPublished - Nov 2017

Bibliographical note

We would like to thank Oscar Ramos-Rodriguez for helping with the execution of the experiments and collections of the bee samples. We would also like to thank Chris Wyatt for providing support for WGCNA analyses and network construction. Many thanks to the Associate Editor and the three anonymous reviewers who provided valuable comments that helped improving the manuscript. This work was funded by a Leverhulme Grant (F/07537/AK) to M.J.F.B. and S.S., which supported I.P. and F.M. F.M. was also supported by a Marie Curie International Incoming Fellowship (FP7-PEOPLE-2013-IIF-625487). A.E.R. and A.P. were supported in part by the Biotechnology and Biological Sciences Research Council (BBSRC), grants BB/K004131/1, BB/F00964X/1 and BB/M025047/1 to A.P.; by the Consejo Nacional de Ciencia y Tecnología Paraguay (CONACYT), grants INVG01-112 (14-INV-088) and PINV15-315 (14-INV-088); and by the National Science Foundation (NSF), grant 1660648.

Data deposition: This project has been deposited at NCBI Gene Expression Omnibus (GEO) database under the accession GSE92730. Additional data sets and codes used in the analyses are available online in the project webpage


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


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