Honey bee queens are vulnerable to heat-induced loss of fertility

Abstract

13All species need to reproduce to maintain viable populations, but heat stress kills sperm cells across the 14 animal kingdom and rising frequencies of heatwaves are a threat to biodiversity. Honey bees (Apis 15 mellifera) are globally distributed micro-livestock; therefore, they could serve as environmental 16 biomonitors for heat-induced reductions in fertility. Here, we found that queens have two potential 17 routes of temperature-stress exposure: within colonies and during routine shipping. Our data suggest 18 that temperatures of 15 to 38°C are safe for queens at a tolerance threshold of 11.5% loss of sperm 19 viability, which is the viability difference between failed and healthy queens collected from beekeepers. 20Heat shock activates expression of specific ATP-independent heat-shock proteins in the spermatheca, 21 which could serve as biomarkers for heat stress. This protein fingerprint may eventually enable surveys 22 with colony losses 41 . Furthermore, internal hive temperatures positively correlate with ambient 46 temperatures above 18°C, and brood nest temperatures can rise upwards of 37°C, both under natural 47 conditions 42 and during simulated heatwaves 43 . Hives occasionally experience spikes of > 40°C 44 , 48 suggesting that queens could be vulnerable to temperature extremes even inside the hive. 49Honey bees have excellent potential for being temperature stress biomonitors. They are a globally 50 distributed, managed species, so they are readily available in almost any geographic region, and they are 51 already accepted as effective biomonitors for pollution 45 . If we begin to observe signs of heat stress in 52 honey bees colonies, that would signal a worrisome risk of reduced reproductive output for ectothermic 53 species. 54Here, we begin to explore honey bees' utility as temperature stress biomonitors. We monitored 55 temperature fluctuations in colonies under extreme weather conditions, establishing that damaging 56 intra-hive temperatures can occur. Next, we tested a range of temperatures and exposure durations to 57 determine thresholds above which queen quality is likely to be compromised. We then investigated the 58 biochemical basis of heat-induced sperm viability reduction in queens and drones using quantitative 59 proteomics, which showed how heat stress alters protein expression of reproductive tissues. The 60 specific set of upregulated proteins we identified may eventually serve as diagnostic tools to elucidate 61 causes of queen failure and eventually enable regional surveys of heat stress as part of an 62 environmental temperature biomonitoring program. 63 Results and Discussion 64 Stored sperm viability of failed and healthy queens 65To establish how much of a reduction in sperm viability is associated with field-observable reduced 66 reproductive output (and associated economic losses for beekeepers), we collected queens rated as 67 'failing' (N = 58) and 'healthy' (N = 55) by beekeepers and measured the queens' stored sperm viability 68

Metagenomic analysis of the honey bee queen microbiome reveals low bacterial diversity and Caudoviricetes phages

“…Honey bee queens were sampled in 2018 from colonies located in Pennsylvania, USA, and in 2019 from colonies in British Columbia, Canada. The samples from both locations are part of previously published datasets (26,27), in which the queens were classified according to their health status. Queens were scored as healthy when they showed no sign of supersedure cells, no drone brood in worker cells, no signs of disease, and had strong worker populations.…”

“…Here we sequenced the metagenomes of 18 queen gut samples from the US and Canada to deeply characterize their microbiome. These queen samples have associated metadata from previous studies (26,27), including both failing and healthy queens. We describe the queen gut microbial community, from bacteria to phages, and investigate the most important factors shaping it.…”

Mating and blood-feeding induce transcriptome changes in the spermathecae of the yellow fever mosquito Aedes aegypti

“…The egg-antigen belongs to the heat-shock protein family. Heat shock proteins have roles in reducing oxidative stress in other insects, including Drososphila 56 and the honey bee 57 .…”