Abstract
Honey bees can host a remarkably large number of different parasites and pathogens, and some are known drivers of recent declines in wild and managed bee populations. Here, we studied the interactions between the fungal pathogen Nosema apis and seminal fluid of the Western honey bee (Apis mellifera). Honey bee seminal fluid contains multiple antimicrobial molecules that kill N. apis spores and we therefore hypothesized that antimicrobial activities of seminal fluid are genetically driven by interactions between honey bee genotype and different N. apis strains/ecotypes, with the virulence of a strain depending on the genotype of their honey bee hosts. Among the antimicrobials, chitinases have been found in honey bee seminal fluid and have the predicted N. apis killing capabilities. We measured chitinase activity in the seminal fluid of eight different colonies. Our results indicate that multiple chitinases are present in seminal fluid, with activity significantly differing between genotypes. We therefore pooled equal numbers of N. apis spores from eight different colonies and exposed subsamples to seminal fluid samples from each of the colonies. We infected males from each colony with seminal fluid exposed spore samples and quantified N. apis infections after 6 days. We found that host colony had a stronger effect compared to seminal fluid treatment, and significantly affected host mortality, infection intensity and parasite prevalence. We also found a significant effect of treatment, as well as a treatment × colony interaction when our data were analyzed ignoring cage as a blocking factor. Our findings provide evidence that N. apis-honey bee interactions are driven by genotypic effects, which could be used in the future for breeding purposes of disease resistant or tolerant honey bee stock.
Highlights
Honey bees are important pollinators of both natural and agricultural ecosystems (Biesmeijer et al, 2006; Klein et al, 2007; Potts et al, 2010; Ollerton et al, 2011)
Recent analyses reported different effects on honey bees when being exposed to multiple environmental stressors including parasites (Bird et al, 2021; Siviter et al, 2021), Nosema infections become more detrimental to honey bees when they coincide with the presence of other environmental stressors such as pesticides (Aufauvre et al, 2012; Grassl et al, 2018; Al Naggar and Baer, 2019)
There are four possible outcomes being that spore virulence is (1) driven entirely by non-genetic factors, i.e., colony resistance is driven by other factors and/or seminal fluid does not have the predicted strain filtering effect, (2) driven by resistance that is defined by host colony with no or minimal filtering effects of seminal fluid, (3) driven by a highly specific filtering effect of seminal fluid with colony having little or no significant effects, and (4) parasite infectivity being determined by significant effects of both colony and seminal fluid identity (Figure 1)
Summary
Honey bees are important pollinators of both natural and agricultural ecosystems (Biesmeijer et al, 2006; Klein et al, 2007; Potts et al, 2010; Ollerton et al, 2011). The presence of innate immunity proteins in seminal fluid (Grassl et al, 2016) provides a possible genomic driver of these interactions and offers the possibility to empirically test these predicted outcomes Disentangling these effects is challenging, and we used a common garden design to separate effects of seminal fluid exposure, host genetics and interactions between them on parasite infectivity and virulence. There are four possible outcomes being that spore virulence is (1) driven entirely by non-genetic factors, i.e., colony resistance is driven by other factors and/or seminal fluid does not have the predicted strain filtering effect, (2) driven by resistance that is defined by host colony with no or minimal filtering effects of seminal fluid, (3) driven by a highly specific filtering effect of seminal fluid with colony having little or no significant effects, and (4) parasite infectivity being determined by significant effects of both colony and seminal fluid identity (Figure 1). We quantified chitinase activity in seminal fluid and hypothesized that activity levels would differ between bee genotypes
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