Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus

Doublet, Vincent; Natsopoulou, Myrsini E.; Zschiesche, Luise; Paxton, Robert J.

doi:10.1016/j.jip.2014.10.007

Cited by 57 publications

(52 citation statements)

References 28 publications

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“…Mechanistically, the lower virulence in sequential compared to simultaneous infections could be related, for example, to reduction in the rate of bacterial invasion to the host's body (Louhi et al, 2015), or to higher efficiency of the host's immune system to F I G U R E 2 Mean survival times (±SE) of rainbow trout previously unexposed (Unexp., open boxes) or exposed to Diplostomum pseudospathaceum (Exposed, grey boxes) when reexposed to three strains of the bacterium Flavobacterium columnare Klemme et al, 2016). Overall, our results add significantly to earlier studies on sequential infections between different parasite taxa, majority of which have used single genotypes/strains (Ben-Ami et al, 2011;Clay, Dhir, et al, 2019;Doublet et al, 2015;Hoverman et al, 2013;Lohr et al, 2010;Marchetto & Power, 2018;Natsopoulou et al, 2015), by emphasizing the importance of variation in infection outcomes depending on the specific G × G parasite combinations. Indeed, combining G × G interactions in multiple parasites with host infection history makes estimation of virulence and virulence evolution increasingly challenging (Karvonen, Jokela, & Laine, 2019).…”

Section: Discussionsupporting

confidence: 68%

Sequential infection can decrease virulence in a fish–bacterium–fluke interaction: Implications for aquaculture disease management

Karvonen

Fenton

Sundberg

2019

Evolutionary Applications

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Hosts are typically infected with multiple strains or genotypes of one or several parasite species. These infections can take place simultaneously, but also at different times, i.e. sequentially, when one of the parasites establishes first. Sequential parasite dynamics are common in nature, but also in intensive farming units such as aquaculture. However, knowledge of effects of previous exposures on virulence of current infections in intensive farming is very limited. This is critical as consecutive epidemics and infection history of a host could underlie failures in management practices and medical intervention of diseases. Here, we explored effects of timing of multiple infections on virulence in two common aquaculture parasites, the bacterium Flavobacterium columnare and the fluke Diplostomum pseudospathaceum. We exposed fish hosts first to flukes and then to bacteria in two separate experiments, altering timing between the infections from few hours to several weeks. We found that both short‐term and long‐term differences in timing of the two infections resulted in significant, genotype‐specific decrease in bacterial virulence. Second, we developed a mathematical model, parameterized from our experimental results, to predict the implications of sequential infections for epidemiological progression of the disease, and levels of fish population suppression, in an aquaculture setting. Predictions of the model showed that sequential exposure of hosts can decrease the population‐level impact of the bacterial epidemic, primarily through the increased recovery rate of sequentially infected hosts, thereby substantially protecting the population from the detrimental impact of infection. However, these effects depended on bacterial strain–fluke genotype combinations, suggesting the genetic composition of the parasite populations can greatly influence the degree of host suppression. Overall, these results suggest that host infection history can have significant consequences for the impact of infection at host population level, potentially shaping parasite epidemiology, disease dynamics and evolution of virulence in farming environments.

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Section: Discussionsupporting

confidence: 68%

Sequential infection can decrease virulence in a fish–bacterium–fluke interaction: Implications for aquaculture disease management

Karvonen

Fenton

Sundberg

2019

Evolutionary Applications

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“…A third possibility is that LSV-2 is directly linked with Nosema , which in turn inhibits DWV replication. Prior establishment in the host ventriculus by Nosema has been shown to inhibit DWV establishment (Doublet et al 2015). Their results demonstrated that prior infection by DWV did not impact N. ceranae , while our survey results suggest that DWV load may negatively impact the establishment of Nosema , as bees free of Nosema had significantly higher DWV load than bees infected with Nosema (Figure 10).…”

Section: Discussionmentioning

confidence: 55%

Multiyear survey targeting disease incidence in US honey bees

et al. 2016

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-The US National Honey Bee Disease Survey sampled colony pests and diseases from 2009 to 2014. We verified the absence of Tropilaelaps spp., the Asian honey bee (Apis cerana ), and slow bee paralysis virus. Endemic health threats were quantified, including Varroa destructor , Nosema spp., and eight honey bee viruses. Varroa loads varied across years, with annual fall peaks; Nosema peaked January to April. Migratory beekeepers had significantly lower Varroa prevalence (84.9 vs. 97.0 %) and loads (3.65 ± 0.28 vs. 5.99 ± 0.22) than stationary operations, while Nosema was more prevalent (59.9 vs. 46.7 %) in migratory colonies. Since 2010, chronic bee paralysis virus prevalence doubled annually. We detected strong positive relationships between V. destructor and Varroa -transmitted viruses, between Nosema and Lake Sinai virus 2, and a positive relationship across several viral pathogens of bees. The results provide a disease baseline to help identify drivers of poor bee health.Apis mellifera / disease survey / pests / parasite / USA

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“…A recent survey suggested that the DWV load may negatively impact establishment of Nosema spp., as Nosema ‐free honey bees had significantly higher DWV loads than Nosema ‐infected honey bees (Traynor et al ., ). The order of infection seems to be important; prior N. ceranae infection inhibited subsequent DWV infection but this was not reciprocal, suggesting asymmetry in the competitive interaction between these pathogens (Doublet et al ., ). In another experiment, N. ceranae fed to emerging bees from a DWV‐infected colony appeared to accelerate DWV replication at early stages of viral infection in a dose‐dependent manner, but not once DWV titers reached a plateau (Zheng et al ., ).…”

Section: What Are the Major Effects Of N Ceranae On Honey Bees?mentioning

confidence: 97%

“…A synergistic effect between N. ceranae and neonicotinoids, first observed under laboratory conditions, causes a significantly higher bee mortality along with a reduction in glucose oxidase activity, which is involved in social immunity through the sterilization of the colony and brood food (Alaux et al ., ). This synergism between neonicotinoids and N. ceranae in adult bees has been confirmed by others (Vidau et al ., ; Aufauvre et al ., ; Doublet et al ., ) and was also observed in field studies demonstrating an indirect effect of imidacloprid on N. ceranae growth, even when honey bees were exposed to levels below those considered harmful (Pettis et al ., ). In contrast with those observations, Gregorc and colleagues () did not detect an effect of a neonicotinoid on N. ceranae growth in laboratory conditions but a minor synergistic toxic effect on the honey bee midgut tissue compared to that of both stressors separately.…”

Section: What Are the Major Effects Of N Ceranae On Honey Bees?mentioning

confidence: 97%

Nosema ceranae in Apis mellifera: a 12 years postdetection perspective

Martín-Hernández

Bartolomé

Chejanovsky

et al. 2018

Environmental Microbiology

166

118

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Nosema ceranae is a hot topic in honey bee health as reflected by numerous papers published every year. This review presents an update of the knowledge generated in the last 12 years in the field of N. ceranae research, addressing the routes of transmission, population structure and genetic diversity. This includes description of how the infection modifies the honey bee's metabolism, the immune response and other vital functions. The effects on individual honey bees will have a direct impact on the colony by leading to losses in the adult's population. The absence of clear clinical signs could keep the infection unnoticed by the beekeeper for long periods. The influence of the environmental conditions, beekeeping practices, bee genetics and the interaction with pesticides and other pathogens will have a direct influence on the prognosis of the disease. This review is approached from the point of view of the Mediterranean countries where the professional beekeeping has a high representation and where this pathogen is reported as an important threat.

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Within-host competition among the honey bees pathogens Nosema ceranae and Deformed wing virus is asymmetric and to the disadvantage of the virus

Cited by 57 publications

References 28 publications

Sequential infection can decrease virulence in a fish–bacterium–fluke interaction: Implications for aquaculture disease management

Sequential infection can decrease virulence in a fish–bacterium–fluke interaction: Implications for aquaculture disease management

Multiyear survey targeting disease incidence in US honey bees

Nosema ceranae in Apis mellifera: a 12 years postdetection perspective

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