Drone honey bees are disproportionately sensitive to abiotic stressors despite expressing high levels of stress response proteins

Alison Mcafee,Bradley N Metz,Joseph P Milone,Leonard J Foster,David R Tarpy

doi:10.1038/s42003-022-03092-7

Abstract

Drone honey bees (Apis mellifera) are the obligate sexual partners of queens, and the availability of healthy, high-quality drones directly affects a queen’s fertility and productivity. Yet, our understanding of how stressors affect adult drone fertility, survival, and physiology is presently limited. Here, we investigated sex biases in susceptibility to abiotic stressors (cold stress, topical imidacloprid exposure, and topical exposure to a realistic cocktail of pesticides). We found that drones (haploid males) were more sensitive to cold and imidacloprid exposure than workers (sterile, diploid females), but the cocktail was not toxic at the concentrations tested. We corroborated this lack of cocktail toxicity with in-hive exposures via pollen feeding. We then used quantitative proteomics to investigate protein expression profiles in the hemolymph of topically exposed workers and drones, and found that 34 proteins were differentially expressed in exposed drones relative to controls, but none were differentially expressed in exposed workers. Contrary to our hypothesis, we show that drones express surprisingly high baseline levels of putative stress response proteins relative to workers. This suggests that drones’ stress tolerance systems are fundamentally rewired relative to workers, and susceptibility to stress depends on more than simply gene dose or allelic diversity.

Highlights

Drone honey bees (Apis mellifera) are the obligate sexual partners of queens, and the availability of healthy, high-quality drones directly affects a queen’s fertility and productivity
Grassl et al.15. found that drones are more sensitive to thiamethoxam than workers, and our previous research shows that drones are more susceptible than workers to heat[10]. This apparent biased sensitivity of haploid male bees to abiotic stressors may be in part explained by an extension of the haploid susceptibility hypothesis, which states that haploid individuals are more susceptible to pathogenic infections, since they have no opportunity for allelic diversity that comes with heterozygosity[16]
We and others have previously reported drone-biased sensitivity to heat[10,11], and Grassl et al identified drone-biased sensitivity to thiamethoxam[15]. To determine if this sex bias exists across other abiotic stressors, we used cage experiments to compare worker and drone sensitivity to cold (4 °C, which acts as a positive control for mortality), imidacloprid (1, 10, and 100 ppm, 2 μl topical exposure in acetone), and a cocktail of the nine compounds frequently found in wax

Summary

Introduction

Drone honey bees (Apis mellifera) are the obligate sexual partners of queens, and the availability of healthy, high-quality drones directly affects a queen’s fertility and productivity. Found that drones are more sensitive to thiamethoxam than workers, and our previous research shows that drones are more susceptible than workers to heat[10] This apparent biased sensitivity of haploid male bees to abiotic stressors may be in part explained by an extension of the haploid susceptibility hypothesis, which states that haploid individuals are more susceptible to pathogenic infections, since they have no opportunity for allelic diversity that comes with heterozygosity[16]. While investigations on honey bee male susceptibility to Nosema[19], as well as immunocompetence of leafcutter ants (Atta colombica)[20], wood ants (Formica exsecta)[21], and bufftailed bumble bees (Bombus terrestris)[22] support the haploid susceptibility hypothesis, research on B. terrestris male susceptibility to Crithidia does not[18] This hypothesis has generally not been discussed in the context of abiotic stress, despite being a relevant challenge

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