Abstract

The health of western honey bee (Apis mellifera) colonies is challenged by the parasitic mite Varroa destructor and the numerous harmful pathogens it vectors. Selective breeding for the naturally occurring social immune trait “hygienic behavior” has emerged as one sustainable approach to reducing the mites’ impact on honey bees. To expand our understanding of hygienic triggers and improve hygienic selection tools, we tested the hypothesis that the cuticular compounds (Z)-10-tritriacontene and (Z)-6-pentadecene, previously associated with unhealthy honey bee brood and/or brood targeted for hygiene, are triggers of honey bee hygienic behavior independent of brood health. In support of our hypothesis, application of synthetic (Z)-10-tritriacontene and (Z)-6-pentadecene onto brood and brood cell caps significantly increased hygienic behavior compared to application of similarly structured hydrocarbon controls (Z)-16-dotriacontene and (Z)-7-pentadecene. Furthermore, we demonstrate a significant positive correlation between colony-level hygienic responses to (Z)-10-tritriacontene and the traditional freeze-killed brood assay for selection of hygienic honey bee stocks. These results confirm biological activity of (Z)-6-pentadecene and reveal (Z)-10-tritriacontene as a novel hygiene trigger. They also support development of improved tools for honey bee colony monitoring and hygienic selection, and thus may accelerate development of honey bee stocks with greater resistance to Varroa and associated pathogens.

Highlights

  • As with other social insects, honey bees are highly susceptible to the horizontal spread of infectious diseases due to close contact, high coefficients of relatedness, and high frequency of social interactions among individuals within a colony[1,2,3]

  • Parasitized and Deformed Wing Virus (DWV)-infected brood have been associated with higher proportions of several unsaturated hydrocarbons including pentadecene, hentriacontene, and tritriacontene[47,49,50,51,52], and specific isomers of these alkenes, including (Z)-6-pentadecene (Z6-C15), (Z)-8-hentriacontene (Z8-C31), and (Z)-10-tritriacontene (Z10-C33; subsequent abbreviations conform to this pattern), have been associated with brood targeted with hygienic behavior[49,50]

  • Hygienic behavior may be stimulated by intraspecific signals through changes www.nature.com/scientificreports in amounts and ratios of naturally occurring native chemicals

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Summary

Introduction

As with other social insects, honey bees are highly susceptible to the horizontal spread of infectious diseases due to close contact, high coefficients of relatedness, and high frequency of social interactions among individuals within a colony[1,2,3]. Hygienic behavior is the detection, uncapping, and removal of diseased or parasite-infested brood from the colony[32,33], and is one of the resistance mechanisms of Varroa’s original host, the eastern honey bee Apis cerana[34] It occurs naturally in A. mellifera at a low frequency and is most commonly observed in worker bees aged 15 to 20 days[35]. HYG bees are selected based on their hygienic removal of freeze-killed brood[36], whereas VSH bees are selected based on their apparent suppression of mite reproduction[37] Both of these stocks have reduced pathogen loads compared to unselected (UNS) colonies[32,37,38], the process of selecting for suppression of mite reproduction is time-consuming and other interventions, including miticides, are still needed to control severe mite infestations in HYG colonies[39,40]. With one notable exception[49], current evidence for relationships between brood hydrocarbons and honey bee hygiene is either correlative or chemically undefined (i.e., cell treatment with brood extracts), suggesting the need for analysis of the effects of direct application of individual chemicals of interest to honey bee brood cells

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