Melissococcus plutonius is a bacterial pathogen that causes epidemic outbreaks of European foulbrood (EFB) in honey bee populations. The pathogenicity of a bacterium depends on its virulence, and understanding the mechanisms influencing virulence may allow for improved disease control and containment. Using a standardized in vitro assay, we demonstrate that virulence varies greatly among sixteen M. plutonius isolates from five European countries. Additionally, we explore the causes of this variation. In this study, virulence was independent of the multilocus sequence type of the tested pathogen, and was not affected by experimental coinfection with Paenibacillus alvei, a bacterium often associated with EFB outbreaks. Virulence in vitro was correlated with the growth dynamics of M. plutonius isolates in artificial medium, and with the presence of a plasmid carrying a gene coding for the putative toxin melissotoxin A. Our results suggest that some M. plutonius strains showed an increased virulence due to the acquisition of a toxin-carrying mobile genetic element. We discuss whether strains with increased virulence play a role in recent EFB outbreaks.
Background
In spite of the implementation of control strategies in honey bee (Apis mellifera) keeping, the invasive parasitic mite Varroa destructor remains one of the main causes of colony losses in numerous countries. Therefore, this parasite represents a serious threat to beekeeping and agro-ecosystems that benefit from the pollination services provided by honey bees. To maintain their stocks, beekeepers have to treat their colonies with acaricides every year. Selecting lineages that are resistant to infestations is deemed to be a more sustainable approach.
Review
Over the last three decades, numerous selection programs have been initiated to improve the host–parasite relationship and to support honey bee survival in the presence of the parasite without the need for acaricide treatments. Although resistance traits have been included in the selection strategy of honey bees, it has not been possible to globally solve the V. destructor problem. In this study, we review the literature on the reasons that have potentially limited the success of such selection programs. We compile the available information to assess the relevance of selected traits and the potential environmental effects that distort trait expression and colony survival. Limitations to the implementation of these traits in the field are also discussed.
Conclusions
Improving our knowledge of the mechanisms underlying resistance to V. destructor to increase trait relevance, optimizing selection programs to reduce environmental effects, and communicating selection outcomes are all crucial to efforts aiming at establishing a balanced relationship between the invasive parasite and its new host.
SUMMARYVarroa destructor is considered the most damaging parasite affecting honeybees (Apis mellifera L.). However, some honeybee populations such as the savannah honeybee (A. m. scutellata) can survive mite infestation without treatment. It is unclear if survival is due to resistance mechanisms decreasing parasite reproduction or to tolerance mechanisms decreasing the detrimental effects of mites on the host. This study investigates both aspects by quantifying the reproductive output of V. destructor and its physiological costs at the individual host level. Costs measured were not consistently lower when compared to susceptible honeybee populations, indicating a lack of tolerance. In contrast, reproduction of V. destructor mites was distinctly lower than in susceptible populations. There was a higher proportion of infertile individuals and the reproductive success of fertile mites was lower than measured to date, even in surviving populations. Our results suggest that survival of savannah honeybees is based on resistance rather than tolerance to this parasite. We identified traits that may be useful for breeding programs aimed at increasing the survival of susceptible populations. African honeybees may have benefited from a lack of human interference, allowing natural selection to shape a population of honeybees that is more resistant to Varroa mite infestation.2
The ectoparasitic mite, Varroa destructor, shifted host from the eastern honeybee, Apis cerana, to the western honeybee, Apis mellifera. Whereas the original host survives infestations by this parasite, they are lethal to colonies of its new host. Here, we investigated a population of A. cerana naturally infested by the V. destructor Korea haplotype that gave rise to the globally invasive mite lineage. Our aim was to better characterize traits that allow for the survival of the original host to infestations by this particular mite haplotype. A known major trait of resistance is the lack of mite reproduction on worker brood in A. cerana. We show that this trait is neither due to a lack of host attractiveness nor of reproduction initiation by the parasite. However, successful mite reproduction was prevented by abnormal host development. Adult A. cerana workers recognized this state and removed hosts and parasites, which greatly affected the fitness of the parasite. These results confirm and complete previous observations of brood susceptibility to infestation in other honeybee host populations, provide new insights into the coevolution between hosts and parasites in this system, and may contribute to mitigating the large‐scale colony losses of A. mellifera due to V. destructor.
In a globalized world, parasites are often brought in contact with new potential hosts. When parasites successfully shift host, severe diseases can emerge at a large cost to society. However, the evolutionary processes leading to successful shifts are rarely understood, hindering risk assessment, prevention, or mitigation of their effects. Here, we screened populations of Varroa destructor, an ectoparasitic mite of the honeybee genus Apis, to investigate their genetic structure and reproductive potential on new and original hosts. From the patterns identified, we deduce the factors that influenced the macro- and microevolutionary processes that led to the structure observed. Among the mite variants identified, we found two genetically similar populations that differed in their reproductive abilities and thus in their host specificity. These lineages could interbreed, which represents a threat due to the possible increased virulence of the parasite on its original host. However, interbreeding was unidirectional from the host-shifted to the nonshifted native mites and could thus lead to speciation of the former. The results improve our understanding of the processes affecting the population structure and evolution of this economically important mite genus and suggest that introgression between shifted and nonshifted lineages may endanger the original host.
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