Vulnerability of honey bee queens to heat-induced loss of fertility

Abstract

All species need to reproduce to maintain viable populations, but heat stress kills sperm cells across the animal kingdom and rising frequencies of heat waves are a threat to biodiversity. Honey bees (Apis mellifera) are globally distributed microlivestock; therefore, they could serve as environmental biomonitors for fertility losses. Here, we found that queens have two potential routes of temperature-stress exposure: within colonies and during routine shipping. Our data suggest that temperatures of 15–38 °C are safe for queens at a tolerance threshold of 11.5% loss of sperm viability, which is the viability difference associated with queen failure in the field. Heat shock activates expression of specific stress-response proteins in the spermatheca, which could serve as molecular biomarkers (indicators) for heat stress. This protein fingerprint may eventually enable surveys for the prevalence of heat-induced loss of sperm viability in diverse landscapes as part of a biomonitoring programme.

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Fig. 1: Observational data on shipping temperatures, hive temperatures and stored sperm viability.
Fig. 2: Viability of stored and ejaculated sperm after temperature stress.
Fig. 3: Sex-biased heat mortality in honey bees, stink bugs and fruit flies.
Fig. 4: Differential protein expression comparing heat-shocked and not heat-shocked reproductive tissues.
Fig. 5: GO term enrichment analyses.
Fig. 6: HSP expression profiles.

Data availability

All raw mass spectrometry data, protein databases and search results are available on PRIDE ProteomeXchange (accession: PXD013728). Figures with associated raw mass spectrometry data include Figs. 46 and Supplementary Fig. 4. Global protein abundances and P values for the laboratory heat-shock comparisons are available in Supplementary Data 1. Source Data for Figs. 1 and 2 are provided as Source Data files. Any other data that support the findings of this study are available from the corresponding author on request.

Code availability

No specialized code central to our conclusions was used in this manuscript. R code for standard statistical analyses and figure generation will be provided upon request.

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Acknowledgements

This work was supported by Natural Sciences and Engineering Research Council of Canada Discovery grant no. 311654-11 and grants from Genome Canada and Genome British Columbia awarded to L.J.F.; Project Apis m grants awarded to A.M., M.M.G. and J.S.P.; and USDA-NIFA grant no. 2016-07962 awarded to J.S.P. and D.R.T. We thank A. Sébastien and M. Jelen for providing us with stink bugs and fruit flies, respectively, for the survival experiments. We also thank Ashurst Bee Company for help with colony heat testing and Kettle Valley Queens, Nicola Valley Honey, Wild Antho, Campbells Gold Honey, Heather Meadows Honey Farm, Six Legs Good Apiaries, Wildwood Queens, Cariboo Honey and Worker Bee Honey Company for donating failed and healthy queens for this research.

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Contributions

A.M. wrote the first draft of the manuscript and revisions, conducted all data analysis, made the figures and performed the proteomics experiments. A.C. and A.M. conducted the failed queen survey, with assistance from H.H. and M.M.G. H.H. and M.M.G. executed the queen shipment temperature tracking. J.M. performed the survival experiments. M.M.G. and J.S.P. performed the drone sperm viability analyses. R.U. contributed the age-matched failed and healthy queens. J.S.P. performed the queen sperm viability measurements across the range of temperatures and measured internal hive temperatures. Grants to D.R.T., J.S.P., M.M.G., A.M. and L.J.F. supported this research. All authors contributed intellectually.

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Correspondence to Leonard J. Foster or M. Marta Guarna or David R. Tarpy.

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J.S.P. owns a honey bee consulting business. All other authors have no competing interests.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–4 and Tables 1 and 2.

Reporting Summary

Supplementary Data 1

This file contains global LFQ protein expression data and GO term enrichment results for ovaries, spermathecae and semen.

Source data

Source Data Fig. 1

Sperm viability data for failed and healthy queens collected from beekeepers, temperature data for shipments and temperature data for hives.

Source Data Fig. 2

Sperm viability data for temperature-stressed queens and drones.

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McAfee, A., Chapman, A., Higo, H. et al. Vulnerability of honey bee queens to heat-induced loss of fertility. Nat Sustain 3, 367–376 (2020). https://doi.org/10.1038/s41893-020-0493-x

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