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Are there Ubiquitous Parasite-driven Major Histocompatibility Complex Selection Mechanisms in Gray Mouse Lemurs?

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Abstract

A major goal of evolutionary biology is to understand how selection drives local adaptation. For example, the major histocompatibility complex (MHC) plays an important role in the immune system, and high levels of MHC variation are thought to be a form of adaptation in natural populations. Individual MHC composition may influence parasite resistance via advantages associated with 1) heterozygosity, because heterozygotes recognize a broader range of different antigens than homozygotes (heterozygote advantage); 2) highly variable amino acid sequences in MHC alleles, allowing individuals to bind a broader spectrum of parasite-derived peptides (divergent-alleles advantage, a mechanistic variant of the heterozygote advantage model); or 3) specific MHC alleles (rare allele advantage or frequency dependent selection). We investigated relationships between gastrointestinal nematode burden and both adaptive immune gene variability (MHC class II DRB) and neutral microsatellites in free-living gray mouse lemurs (Microcebus murinus) native to a dry deciduous forest population in western Madagascar to test these hypotheses. The individual MHC composition was related to parasite infestation. Specific MHC alleles were involved in parasite resistance and the presence of common alleles negatively influenced infestation intensity. We found no support for the heterozygote advantage hypothesis, but we did find support for the divergent-MHC allele advantage hypothesis: Individuals with very divergent MHC alleles carried fewer and less intense nematode infestations than individuals with more similar alleles in the more variable dry deciduous forest population. These results indicate that intestinal parasites are important selection pressures under natural conditions and suggest that different selection mechanisms are not mutually exclusive. In contrast, we detected no association between neutral overall individual genetic diversity (measured via 17 microsatellites) and parasite load. Finally, we investigated the ubiquity of parasite-driven selection mechanisms by comparing our results with a previous study of a mouse lemur population from the climatically different littoral forest in southeastern Madagascar, ca. 500 km away. This revealed that different specific MHC alleles were involved in parasite resistance in the 2 habitats, showing that gene-parasite associations are not consistent between populations.

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Acknowledgments

We thank the late B. Rakotosamimanana, J. G. Ganzhorn, P. M. Kappeler, R. Rasoloarison, and L. Razafimanantsoa, and the following institutions for their authorization or support of our work in Madagascar: Commission Tripartite of the Malagasy Government, Laboratoire de Primatologie et des Vertébrés de l´Université d´Antananarivo, Parc Botanique et Zoologique de Tsimbazaza, Ministère pour la Production Animale, Département des Eaux et Forêts, Centre de Formation Professionnelle Forestière (CFPF) de Morondava, German Primate Center. All research reported in this manuscript adhered to the legal requirements of Germany and Madagascar and complied with the protocols approved by the appropriate institutional Animal Care and Use Committee (Bundesministerium für Naturschutz (BfN), Germany; Ministère de l’Environnement et des Eaux et Forêts (MINEEF), Madagascar). Thoralf Borchardt helped with the field work. We thank I. Tomaschweski for technical assistance in the lab, Julia Schad for providing her photos of parasites of the littoral forests and assistance in the comparison of parasite data, and Catherine Reid for language corrections. Three anonymous reviewers and Joanna Setchell provided valuable comments on a previous version of the manuscript. This study was made possible by financial support of the German Science Foundation (DFG).

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  1. Department of Evolutionary Genetics, Leibniz Institute for Zoo and Wildlife Research (IZW), 10315, Berlin, Germany

    Nina Schwensow & Simone Sommer

  2. Department of Behavioral Ecology & Sociobiology, Leibniz Institute for Primate Research (DPZ), 37077, Göttingen, Germany

    Manfred Eberle

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Schwensow, N., Eberle, M. & Sommer, S. Are there Ubiquitous Parasite-driven Major Histocompatibility Complex Selection Mechanisms in Gray Mouse Lemurs?. Int J Primatol 31, 519–537 (2010). https://doi.org/10.1007/s10764-010-9411-9

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