There is clear evidence for sublethal effects of neonicotinoid insecticides on non-target ecosystem service-providing insects. However, their possible impact on male insect reproduction is currently unknown, despite the key role of sex. Here, we show that two neonicotinoids (4.5 ppb thiamethoxam and 1.5 ppb clothianidin) significantly reduce the reproductive capacity of male honeybees (drones), Apis mellifera . Drones were obtained from colonies exposed to the neonicotinoid insecticides or controls, and subsequently maintained in laboratory cages until they reached sexual maturity. While no significant effects were observed for male teneral (newly emerged adult) body mass and sperm quantity, the data clearly showed reduced drone lifespan, as well as reduced sperm viability (percentage living versus dead) and living sperm quantity by 39%. Our results demonstrate for the first time that neonicotinoid insecticides can negatively affect male insect reproductive capacity, and provide a possible mechanistic explanation for managed honeybee queen failure and wild insect pollinator decline. The widespread prophylactic use of neonicotinoids may have previously overlooked inadvertent contraceptive effects on non-target insects, thereby limiting conservation efforts.

The Western honeybee, Apis mellifera, is the most important managed pollinator globally and has recently experienced unsustainably high colony losses. Synergistic interactions among stressors are believed to be primarily responsible. However, despite clear evidence of strong effect on honeybee longevity of widely-employed neonicotinoid insecticides and of the ubiquitous ectoparasitic mite Varroa destructor, no data exist to show synergistic effects between these two stressors. Even though neonicotinoids had no significant impact by themselves, we here show for the first time a synergistic time-lag interaction between mites and neonicotinoids that resulted in significantly reduced survival of long-lived winter honeybees. Even though these mites are potent vectors of viruses, the virus-insecticide interaction had no significant impact. The data suggest a previously overlooked mechanism possibly explaining recent unsustainably high losses of managed A. mellifera honeybee colonies in many regions of the world. Future mitigation efforts should concentrate on developing sustainable agro-ecosystem management schemes that incorporate reduced use of neonicotinoids and sustainable solutions for V. destructor mites.

Neonicotinoid insecticides are currently of major concern for the health of wild and managed insects that provide key ecosystem services like pollination. Even though sublethal effects of neonicotinoids are well known, there is surprisingly little information on how they possibly impact developmental stability, and to what extent genetics are involved. This holds especially true for haploid individuals because they are hemizygous at detoxification loci and may be more susceptible. Here we take advantage of haplodiploidy in Western honey bees, Apis mellifera, to show for the first time that neonicotinoids affect developmental stability in diploid females (workers), and that haploid males (drones) are even more susceptible. Phenotypic fore wing venation abnormalities and fluctuating wing asymmetry, as measures of developmental instability, were significantly increased under field-realistic neonicotinoid-exposure of colonies. The higher susceptibility of haploid drones suggests that heterozygosity can play a key role in the ability to buffer the sublethal effects of neonicotinoids. Aiming to improve conservation efforts, our findings highlight the urgent need to better understand the role that genetics plays at enabling non-target organisms to cope with insecticide exposure.

Agricultural chemicals such as neonicotinoid insecticides are believed to be one important factor responsible for the recent reduction in health of pollinating insects like the western honeybee Apis mellifera. However, effects of neonicotinoids on male (drone) honeybee health remain severely understudied. We examined for the first time the multidimensional effects of field‐realistic concentrations of two common neonicotinoid insecticides (thiamethoxam and clothianidin) on drone honeybee survival, behaviour and physiology using individuals reared and maintained as adults in the field. Our data showed that neonicotinoids reduced honeybee drone survival by 51%, increased drifting behaviour to non‐maternal colonies by 100%, delayed flight activities by 3 days and reduced number of living sperm by 28%. However, they did not influence the sperm concentration produced by the drones, the strength of the drone's maternal colonies or the total number of drones produced by those colonies. Policy implications. Our study demonstrated that neonicotinoids can elicit a diverse array of lethal (survival) and sublethal (behaviour, reproductive physiology) effects on male honeybees Apis mellifera in the field. These findings should be considered by policy makers looking to adopt and implement science‐based, holistic risk assessments to more comprehensively assess effects of chemicals on important ecosystem service providing insects like the honeybee. To date, risk assessment schemes do not specifically address potential effects on male bees.