Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation

Ian M. Traniello, Syed Abbas Bukhari, Jessica Kevill, Amy Cash Ahmed, Adam R. Hamilton, Nicholas L. Naeger, Declan C. Schroeder, Gene E. Robinson

Research output: Contribution to journalArticlepeer-review

3 Scopus citations

Abstract

Crop pollination by the western honey bee Apis mellifera is vital to agriculture but threatened by alarmingly high levels of colony mortality, especially in Europe and North America. Colony loss is due, in part, to the high viral loads of Deformed wing virus (DWV), transmitted by the ectoparasitic mite Varroa destructor, especially throughout the overwintering period of a honey bee colony. Covert DWV infection is commonplace and has been causally linked to precocious foraging, which itself has been linked to colony loss. Taking advantage of four brain transcriptome studies that unexpectedly revealed evidence of covert DWV-A infection, we set out to explore whether this effect is due to DWV-A mimicking naturally occurring changes in brain gene expression that are associated with behavioral maturation. Consistent with this hypothesis, we found that brain gene expression profiles of DWV-A infected bees resembled those of foragers, even in individuals that were much younger than typical foragers. In addition, brain transcriptional regulatory network analysis revealed a positive association between DWV-A infection and transcription factors previously associated with honey bee foraging behavior. Surprisingly, single-cell RNA-Sequencing implicated glia, not neurons, in this effect; there are relatively few glial cells in the insect brain and they are rarely associated with behavioral plasticity. Covert DWV-A infection also has been linked to impaired learning, which together with precocious foraging can lead to increased occurrence of infected bees from one colony mistakenly entering another colony, especially under crowded modern apiary conditions. These findings provide new insights into the mechanisms by which DWV-A affects honey bee health and colony survival.

Original languageEnglish (US)
Article number3101
JournalScientific reports
Volume10
Issue number1
DOIs
StatePublished - Dec 1 2020

Bibliographical note

Funding Information:
We thank D. Charlie Nye and Alison Sankey for beekeeping assistance; Drs. Sihai Dave Zhao, Michael Saul and Chris Fields for helpful discussions that inspired this project; and members of the Robinson Lab for feedback leading to considerable improvements of this manuscript. This research was funded by grant SFLife 291812 from the Simons Foundation, an NIH Pioneer Award (DP1 OD006416), an R01 from the National Institute of General Medical Sciences (#R01-GM117467), the Carl R. Woese Institute for Genomic Biology at the University of Illinois at Urbana-Champaign (all to G.E.R), and the Bee Disease Insurance LTD (to D.C.S).

Publisher Copyright:
© 2020, The Author(s).

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