Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease

There is increasing appreciation that hosts in natural populations are subject to infection by multiple parasite species. Yet the epidemiological and ecological processes determining the outcome of mixed infections are poorly understood. Here, we use two intracellular gut parasites (Microsporidia),...

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Bibliographic Details
Published in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 2015-01, Vol.282 (1798), p.20141896-20141896
Main Authors: Natsopoulou, Myrsini E., McMahon, Dino P., Doublet, Vincent, Bryden, John, Paxton, Robert J.
Format: Article
Language:English
Subjects:
Animals
Apis mellifera
Bees - parasitology
Co-Infection
Host
Host-Parasite Interactions
Intestines - parasitology
Introduced Species
Microsporidia
Nosema
Nosema - physiology
Nosema apis
Parasite
Priority Effect
Species Specificity
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Summary:There is increasing appreciation that hosts in natural populations are subject to infection by multiple parasite species. Yet the epidemiological and ecological processes determining the outcome of mixed infections are poorly understood. Here, we use two intracellular gut parasites (Microsporidia), one exotic and one co-evolved in the western honeybee (Apis mellifera), in an experiment in which either one or both parasites were administered either simultaneously or sequentially. We provide clear evidence of within-host competition; order of infection was an important determinant of the competitive outcome between parasites, with the first parasite significantly inhibiting the growth of the second, regardless of species. However, the strength of this ‘priority effect’ was highly asymmetric, with the exotic Nosema ceranae exhibiting stronger inhibition of Nosema apis than vice versa. Our results reveal an unusual asymmetry in parasite competition that is dependent on order of infection. When incorporated into a mathematical model of disease prevalence, we find asymmetric competition to be an important predictor of the patterns of parasite prevalence found in nature. Our findings demonstrate the wider significance of complex multi-host–multi-parasite interactions as drivers of host–pathogen community structure.
ISSN:0962-8452
1471-2954
DOI:10.1098/rspb.2014.1896