title: Interspecific competition in honeybee intracellular gut parasites is asymmetric and favours the spread of an emerging infectious disease.
abstract: 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.
authors.affiliation: Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 8, Halle (Saale) 06120, Germany myrsini.natsopoulou@zoologie.uni-halle.de.
authors.forename: Myrsini E
authors.initials: ME
authors.lastname: Natsopoulou
authors.affiliation: Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 8, Halle (Saale) 06120, Germany School of Biological Sciences, MBC, Queen's University Belfast, Belfast BT9 7BL, UK Institute of Biology, Freie Universität Berlin, Schwendenerstr. 1, Berlin 14195, Germany Department for Materials and Environment, BAM Federal Institute for Materials Research and Testing, Unter den Eichen 87, Berlin 12205, Germany.
authors.forename: Dino P
authors.initials: DP
authors.lastname: McMahon
authors.affiliation: Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 8, Halle (Saale) 06120, Germany German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig 04103, Germany.
authors.forename: Vincent
authors.initials: V
authors.lastname: Doublet
authors.affiliation: School of Biological Sciences, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK.
authors.forename: John
authors.initials: J
authors.lastname: Bryden
authors.affiliation: Institut für Biologie, Martin-Luther-Universität Halle-Wittenberg, Hoher Weg 8, Halle (Saale) 06120, Germany School of Biological Sciences, MBC, Queen's University Belfast, Belfast BT9 7BL, UK German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig 04103, Germany.
authors.forename: Robert J
authors.initials: RJ
authors.lastname: Paxton
mesh_terms: D000818:Animals; D001516:Bees / Q000469:parasitology*; D006790:Host-Parasite Interactions; D007422:Intestines / Q000469:parasitology; D058865:Introduced Species; D016818:Nosema / Q000502:physiology*; D013045:Species Specificity
keywords: Apis mellifera; Microsporidia; co-infection; host; parasite; priority effect