Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera)

McAfee, Alison; Chapman, Abigail; Pettis, Jeffery S.; Foster, Leonard J.

doi:10.1038/s42003-020-01586-w

Cited by 38 publications

(74 citation statements)

References 66 publications

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“…1c). However, upon inspection of proteins quanti ed within the spermathecal uid, we found that one of the six proteins signi cantly correlating with sperm viability (5% false discovery rate) was Mellitin, which is the main protein component of honey bee venom (Table 2), and which we have not observed in our previous spermatheca proteomics dataset [21]. Here, abundance of Mellitin is inversely linked to sperm viability, strongly suggesting that venom contamination during the dissection process impaired our ability to detect differences in sperm viability between experimental groups.…”

Section: No Direct Effects Of Temperature Stress On Non-destructive Qmentioning

confidence: 66%

“…mM Na 3 C 6 H 5 O 7 ) and sperm viability was measured using dual uorescent staining exactly as previously described [21]. Two days after queens were sacri ced, we returned to the nucs to sample remaining eggs as already described, destroy any queen cells that had been built, normalize colony populations, and introduce new adult queens for the next round of the queen stress trial.…”

Section: Temperature Stress Eld Trialmentioning

confidence: 99%

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Queens, but not their stored sperm, are resilient to temperature stress

McAfee¹,

Foster²

2021

Preprint

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Abiotic stressors such as extreme temperatures can reduce stored sperm viability within queen honey bees. However, little is known about how thermal stress may directly impact queen performance or other maternal quality metrics, such as queen mass, egg laying rate, and development of embryos within eggs. Here, in a blind field trial, we recorded laying pattern, queen mass, and average callow worker mass before and after exposing queens to a cold temperature (4°C, 2 h), hot temperature (42°C, 2 h), and hive temperature (33°C) to serve as a handling control. We then used proteomics to investigate potential vertical effects of maternal temperature stress on embryos, as well as to measure the abundance of previously determined protein markers for temperature stress in the spermathecal fluid. We found no significant effect of abiotic stress on any of the metrics we recorded. These data suggest that there are likely no lasting maternal effects of temperature stress on honey bee queens, and that the queens themselves are highly stress tolerant, but not their stored sperm.

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Section: No Direct Effects Of Temperature Stress On Non-destructive Qmentioning

confidence: 66%

Section: Temperature Stress Eld Trialmentioning

confidence: 99%

Queens, but not their stored sperm, are resilient to temperature stress

McAfee¹,

Foster²

2021

Preprint

Self Cite

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“…Spermathecae were removed from the abdomen with forceps and blotted dry on a Kimwipe, then clean forceps were used to gently remove the tracheal net surrounding the spermatheca. The spermatheca was then lysed in an Ependorf tube containing 100 μl Buffer D and spermathecal fluid proteins were extracted for mass spectrometry analysis exactly as previously described [50].…”

Section: Methodsmentioning

confidence: 99%

“…Proteins were extracted, digested, and purified from spermathecal fluid exactly as previously described [49, 50]. Briefly, sperm cells were spun down from the Buffer D-diluted spermathecal fluid solution and soluble proteins in the supernatant were precipitated with acetone.…”

Section: Methodsmentioning

confidence: 99%

Honey bee queen health is unaffected by contact exposure to pesticides commonly found in beeswax

McAfee

Milone

Metz

et al. 2021

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Honey bee queen health is crucial for colony health and productivity, and pesticides have been previously associated with queen loss and premature supersedure. Prior research has investigated the effects of indirect pesticide exposure on queens via workers, as well as direct effects on queens during development. However, as adults, queens are in constant contact with wax as they walk on comb and lay eggs; therefore, direct pesticide contact with adult queens is a relevant but seldom investigated exposure route. Here, we conducted laboratory and field experiments to investigate the impacts of topical pesticide exposure on adult queens. We tested dose-response relationships of six pesticides commonly found in wax: coumaphos, tau-fluvalinate, atrazine, 2,4-DMPF, chlorpyriphos, chlorothalonil, and a cocktail of all six, each dosed up to 32 times the concentrations typically found in wax. We found no effect of any treatment on queen mass or sperm viability. Furthermore, none of the 1,568 proteins quantified in the queens' fat bodies (a major site of detoxification enzyme production) were differentially expressed. In a field trial with N = 30 queens exposed to either a handling control, a solvent control, or a pesticide cocktail, we again found no impact on queen egg-laying pattern, mass, or emergence mass of daughter workers. Further, of the 3,127 proteins identified in fluid from the spermatheca (sperm storage organ), none were differentially expressed. These experiments consistently show that at realistic exposure levels, pesticides commonly found in wax have no direct impact on queen performance, reproduction, or quality metrics. We suggest that previously reported associations between high levels of pesticide residues in wax and queen failure are most likely driven by indirect effects of worker exposure (either through wax or other hive products) on queen care or queen perception.

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“…Examination of previously published proteomic and transcriptomic data from mated and unmated queen spermathecae, in the absence of identifiable infection, revealed no obvious decrease in the constitutive expression of immune related genes in mated queens, as might be expected if a trade-off was occurring (see Supplementary Fig S1 ). However, we have previously shown that lysozyme, an immune effector, is negatively correlated with stored sperm viability in honey bee queens and that failing queens, even without symptoms of viral infection, have significantly higher titers of black queen cell virus (BQCV) and sacbrood virus (SBV) 33 . This suggests that immune activation and reproduction are negatively associated in honey bee queens, at least in terms of sperm maintenance, but the relationship between immunity and ovary function has not yet been explored.…”

Section: Introductionmentioning

confidence: 99%

Fertility costs of cryptic viral infections in a model social insect

Chapman

Amiri

Han

et al. 2021

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Declining global insect populations emphasize the importance of understanding the drivers underlying reductions in insect fitness. Many insects are subject to a trade-off between reproduction and immune activity, meaning that infections can have indirect impacts on fecundity, even in the absence of overt symptoms. While eusocial insects have escaped a broader trade-off between reproduction and lifespan, our results suggest that honey bees, a model Hymenopteran, are susceptible to reproduction-immunity compromises. We report that natural viral infection is associated with decreased ovary mass and upregulation of heat-shock proteins (HSPs) which are part of the honey bee's antiviral response. Failed (poor quality) queens sampled from a wide geographic range have higher levels of viral infection, smaller ovaries, and altered ovarian protein composition, with over 20% of proteins differentially expressed. Significantly reduced levels of the yolk-protein precursor vitellogenin in the ovaries indicate a direct decline in fertility. We experimentally infected queens with Israeli acute paralysis virus and, as expected, infected queens exhibited significantly lower vitellogenin expression and higher HSP expression, confirming a causal relationship between viral infection and genes involved in fertility and immunity. The link between ovary size and queen failure could not be explained by other abiotic stressors. These findings suggest that viral infections occurring naturally in the field are compromising reproductive success, even among social insects.

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Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera)

Cited by 38 publications

References 66 publications

Queens, but not their stored sperm, are resilient to temperature stress

Queens, but not their stored sperm, are resilient to temperature stress

Honey bee queen health is unaffected by contact exposure to pesticides commonly found in beeswax

Fertility costs of cryptic viral infections in a model social insect

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