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Does the parasite-mediated selection drive the MHC class IIB diversity in wild populations of European chub (Squalius cephalus)?

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Abstract

The genes of major histocompatibility complex (MHC) provide an excellent opportunity to study host–parasite relationships because they are expected to evolve in response to parasites and variation in parasite communities. In this study, we investigated the potential role of parasite-mediated selection acting on MHC class IIB (DAB) genes in European chub (Squalius cephalus) natural populations. We found significant differences between populations in metazoan parasites, neutral and adaptive genetic diversities. The analyses based on pairwise data revealed that populations with dissimilar MHC allelic profiles were geographically distant populations with significantly different diversity in microsatellites and a dissimilar composition of parasite communities. The results from the generalized estimating equations method (GEE) on the level of individuals revealed that metazoan parasite load in European chub was influenced by the diversity of DAB alleles as well as by the diversity of neutral genetic markers and host traits reflecting condition and immunocompetence. The multivariate co-inertia analysis showed specific associations between DAB alleles and parasite species. DAB1-like alleles were more involved in associations with ectoparasites, while DAB3-like alleles were positively associated with endoparasites which could suggest potential differences between DAB genes caused by different selection pressure. Our study revealed that parasite-mediated selection is not the only variable affecting MHC diversity in European chub; however, we strongly support the role of neutral processes as the main driver of DAB diversity across populations. In addition, our study contributes to the understanding of the evolution of MHC genes in wild living fish.

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Acknowledgments

We would like to thank the group from the Department of Fish Ecology, Institute of Vertebrate Biology, Academy of Sciences (Czech Republic); Teodora Trichkova and Milen Vassilev from the Institute of Zoology, Bulgarian Academy of Sciences (Bulgaria); Alexis Ribas Salvador from the Laboratory of Parasitology, University of Barcelona and Antoni Arrizabalaga, responsible for the Museu de Granollers Ciències Naturals “La Tela” (Spain); André Gilles, René Chappaz and their co-workers from Université de Provence Aix- Marseille 1 (France); Paolo Galli from the Department of Biotechnology and Biosciences, University of Milano-Bicocca (Italy); Jussi Pennanen, Finnish Game and Fisheries Research Institute, Helsinki (Finland); and Miroslaw Przybylski, Grziegorz Zieba from the University of Lodz, Lodz (Poland) for their help with fish sampling in the different sampling localities and the opportunity to use their laboratories. We also thank all colleagues from the Laboratory of Parasitology, Faculty of Science, Masaryk University, Brno (Czech Republic) for their help with molecular techniques and fish dissection. We are very grateful to Matthew Nicholls for the English revision of the final version. The field work and travel costs were funded by the Czech Science Foundation, Project No. 524/07/0188. The analyses were funded by the Czech Science Foundation, project No. P505/12/G112 (ECIP). The sponsors had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Authors’ contributions

AŠ conceived and designed the experiments. JJ and MS analyzed the data. MS and AŠ wrote the paper.

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Authors and Affiliations

  1. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137, Brno, Czech Republic

    Mária Seifertová & Andrea Šimková

  2. Institute of Biostatistics and Analyses, Faculty of Medicine and Faculty of Science, Masaryk University, Kamenice 126/3, 625 00, Brno, Czech Republic

    Jiří Jarkovský

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  1. Mária Seifertová
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Figure S1

The distribution of Sqce-DAB alleles and their observed frequencies in each fish population. The frequency of MHC class IIB alleles (DAB1-like alleles in black and DAB3-like alleles in gray) is expressed as the proportion of individuals with a given DAB allele in each of 15 populations of European chub. See Table 1 for population abbreviations. The DAB alleles present in four lineages are shown with an asterisk, the alleles present in three lineages are shown with a circle, and the alleles present in two lineages are shown with +. (GIF 125 kb)

High resolution image (TIF 905 kb)

Table S1

List of metazoan parasite species identified in 15 populations of Squalius cephalus in European rivers. Parasite intensity of infection (mean number of metazoan parasites per infected host) is included. Data on parasite species are from Seifertová et al. (2008). (DOC 165 kb)

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Seifertová, M., Jarkovský, J. & Šimková, A. Does the parasite-mediated selection drive the MHC class IIB diversity in wild populations of European chub (Squalius cephalus)?. Parasitol Res 115, 1401–1415 (2016). https://doi.org/10.1007/s00436-015-4874-4

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