Contents lists available at ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid Research paper Parasite infection of specific host genotypes relates to changes in prevalence in two natural populations of bumblebees Oliver Manlik ⁎ , Regula Schmid-Hempel, Paul Schmid-Hempel ETH Zurich, Institute of Integrative Biology (IBZ), ETH-Zentrum CHN, Universitätsstrasse 16, CH-8092 Zurich, Switzerland ARTICLE INFO Keywords: Mitochondrial DNA Bombus terrestris Host-parasite interaction Coevolution Evolutionary genetics Social insect ABSTRACT The antagonistic relationship between parasites and their hosts is strongly influenced by genotype-by-genotype interactions. Defense against parasitism is commonly studied in the context of immune system-based mechan- isms and, thus, the focus in the search for candidate genes in host-parasite interactions is often on immune genes. In this study, we investigated the association between prevalence of parasite infection and host mitochondrial DNA (mtDNA) haplotypes in two natural populations of bumblebees (Bombus terrestris). The two most common haplotypes of the host populations, termed A and B, differ by a single nonsynonymous nucleotide substitution within the coding region of cytochrome oxidase I, an important player in metabolic pathways. We screened infection by Nosema bombi, a common endoparasite of bumblebees, and the corresponding host mtDNA-hap- lotype frequencies in over 1400 bumblebees between 2000 and 2010. The island population of Gotland showed lower mtDNA diversity compared to the mainland population in Switzerland. Over time, we observed large fluctuations in infection prevalence, as well as variation in host haplotype frequencies in both populations. Our long-term observation revealed that N. bombi infection of specific host genotypes is transient: We found that with increasing infection prevalence, proportionally more individuals with haplotype B, but fewer individuals with haplotype A were infected. This suggests that the presence of N. bombi in specific host genotypes relates to infection prevalence. This may be a result of parasite competition, or differential resilience of host types to ward off infections. The findings highlight the important role of host mtDNA haplotypes in the interaction with parasites. 1. Introduction The genetic interaction between hosts and parasites is key to the dynamics of a host-parasite system and to understand how diseases spread. The relationship between susceptibility to parasite infection and genetic diversity was noticed by Elton (1958). Initially, this insight was based on the observation that crops grown in genetically homogeneous monocultures are typically more susceptible to the spread of diseases than genetically mixed cultures (e.g. Browning and Frey, 1969; Leonard, 1969; Wolfe, 1985; McDonald et al., 1988; Garrett and Mundt, 1999, Zhu et al., 2000, Mundt, 2002, Pilet et al., 2006). The relation- ship between genetic diversity of the host local population (i.e. the colony) and parasitic infection has also been shown in social insects (Hughes and Boomsma, 2004; Reber et al., 2008), including bum- blebees (Liersch and Schmid-Hempel, 1998, Baer and Schmid-Hempel, 1999). Furthermore, colony fitness in bumblebees was found to be correlated with particular mtDNA haplotypes (Johnson et al., 2011). In particular, Baer and Schmid-Hempel (1999) showed that infection load and prevalence of Crithidia bombi (Trypanosomatidae), a common parasite of bumblebees, is lower with higher genetic variation within colonies of its host, Bombus terrestris. In fact, genetically het- erogeneous colonies of B. terrestris harbored generally lower pathogen loads, including lower loads of Nosema bombi (Microsporidia) (Liersch and Schmid-Hempel, 1998, Baer and Schmid-Hempel, 1999). Experi- mental infections of Bombus spp. with N. bombi have furthermore shown that the success of infecting different colonies depends on the source of the parasite's spores (Schmid-Hempel and Loosli, 1998). That study also showed that variation among conspecific colonies had a greater effect on susceptibility to N. bombi than variation across host species. To- gether, this suggests a genotype-genotype interaction between parasite strain (or genotype, respectively) and host colony (representing a host genetic background); this interaction affects the prevalence, infectivity and/or observed virulence effects of N. bombi. Further evidence has come from several additional studies (Schmid-Hempel and Schmid- Hempel, 1993; Schmid-Hempel et al., 1999; Imhoof and Schmid- Hempel, 1998; Schmid-Hempel, 2000). Yet, to date, variation in https://doi.org/10.1016/j.meegid.2017.11.019 Received 4 July 2017; Received in revised form 16 October 2017; Accepted 6 November 2017 ⁎ Corresponding author at: Evolution and Ecology Research Centre, School of Biological Earth and Environmental Science, University of New South Wales, Sydney, NSW 2052, Australia. E-mail address: o.manlik@unsw.edu.au (O. Manlik). Infection, Genetics and Evolution 56 (2017) 125–132 Available online 16 November 2017 1567-1348/ © 2017 Elsevier B.V. All rights reserved. T