Mixed infections illustrate virulence differences between host-specific bee pathogens

Authors: Klinger, Ellen; VOJVODIC, SVETLANA - University Of Arizona; DeGrandi-Hoffman, Gloria; WELKER, DENNIS - Utah State University; James, Rosalind

Submitted to: Journal of Invertebrate Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/5/2015
Publication Date: 7/15/2015
Publication URL: http://doi:10.1016/j.jip.2015.05.003
Citation: Klinger, E.G., Vojvodic, S., Hoffman, G.D., Welker, D., James, R.R. 2015. Mixed infections illustrate virulence differences between host-specific bee pathogens. Journal of Invertebrate Pathology. 129:28-35. https://doi.org/10.1016/j.jip.2015.05.0.
DOI: https://doi.org/10.1016/j.jip.2015.05.0

Interpretive Summary: Recent concerns about colony collapse disorder in honey bees has brought attention to the fact that animals often become infected with more than one pathogen at a time, and bees are no exception to this. However, we know little about how pathogens affect each other inside a host, nor do we know how these interactions affect host health, for any host, let alone bees. These interactions are complex, and so mathematical models have been used to improve our understanding, but real data are needed to test some of the hypotheses generated by the models, so we set out to do just that. We tested two common models for mixed infection models, one called superinfection and the other called co-infection. We then set out to determine which model best describes the chalkbrood diseases affecting bees. We tested three pathogens that cause chalkbrood in two different bees, the honey bee and the alfalfa leafcutting bee. We found that the mortality due to disease was the same, whether a bee was exposed to one versus two pathogens. However, pathogen growth within the sick bee was different. In tests with honey bees, only the most virulent pathogen was present inside the host at the time the bee died. This result fits the superinfection model. In tests with the alfalfa leafcutting bee, our results fit the other model, the co-infection model. When this was exposed to two pathogens at once, both pathogens were found co-infecting the sick bees. Thus, competition between the pathogens was different in the two kinds of bees. In addition, we found that the most virulent pathogen in honey bees did not infect the alfalfa leafcutting bee, and vice versa. Thus, the highly virulent pathogens were very host-specific.

Technical Abstract: Little is known about multiple-pathogen systems in any host, let alone bees. Understanding host-pathogen interactions is critical to understanding ecosystems and evolutionary biology. However, these interactions are complex, and more so when multiple pathogens infect the same host. Mathematical models help facilitate our understanding of these evolutionary dynamics, but empirical data are needed to test model assumptions and predictions. We used two common theoretical models regarding mixed infections (superinfection and co-infection) to determine which best described a group of fungi closely associated with bees, the Ascosphaera. In addition, we evaluated the evolutionary hypothesis that phylogenetic relatedness can predict whether two pathogens co-exist within a host as a superinfection vs. co-infection. We tested three fungal species, Ascosphaera apis, Ascosphaera aggregata and Ascosphaera larvis, in two bee hosts (Apis mellifera and Megachile rotundata). Bee survival was not significantly different in mixed infections vs. solo infections with the most virulent pathogen, for either host, but fungal growth within the host was significantly altered by mixed infections. In the host A. mellifera, only the most virulent pathogen was present in the host post-infection (indicating a superinfection). In M. rotundata, the most virulent pathogen was present with the lesser-virulent one (indicating a co-infection). There was no evidence that phylogenetic similarity in this genus led to co-infections over superinfections. The results of mixed infections were host-specific, indicating strong host specificity among the pathogenic Ascosphaera.