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Patterns of evolution in MHC class II DQA and DQB exon 2 genes of Alpine mountain hares, Lepus timidus varronis, and sympatric and parapatric brown hares, L. europaeus, from Switzerland

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Abstract

In natural populations, hybridization is known to occur between a wide range of species. However, its evolutionary significance is less clear. Genes involved in fighting pathogens are considered excellent candidates for studying adaptive introgression, although both introgression and balancing selection can generate similar patterns of diversity and differentiation. Here, we compared DQA and DQB MHC class II and microsatellite allelic diversity of sympatric and parapatric mountain (Lepus timidus) and brown hare (L. europaeus) populations from Switzerland. We detected higher genetic diversity in brown hares compared to mountain hares at both MHC and microsatellite loci. We consider the observed patterns of microsatellite diversity both for L. europaeus and L. timidus as result of stochastic demographic processes while the pattern of MHC polymorphism of the studied hare populations can be explained by pathogen-driven selection. Rare bidirectional gene flow between both hare species seems to occur specifically for MHC alleles. However, the high number of shared alleles showing similar high frequency in both species suggests that reciprocally exchanged MHC alleles are being maintained via balancing selection. Adaptation to similar pathogen communities can also lead to parallel selection of MHC alleles. Positive selection, recombination and mutations have played different roles in shaping the patterns of MHC allelic diversity in and differentiation between both species. Results for the latter evolutionary forces do not show a better matching between the sympatric populations compared to the parapatric ones, suggesting a minor role of introgression for the observed evolutionary patterns of the studied hare species.

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Acknowledgements

We thank A. Haiden for supporting with laboratory work, as well as the Swiss hunters, and P. Ratti, (Chur, Switzerland), M. Giaccometti (Stampa), Ch. Rühlé (St. Gallen, Switzerland), G. Haerer (Illnau, Switzerland), and K. Hackländer (Vienna, Austria) for help with organizing genetic samples in the late 1990ie and early 2000s. Partial financial support was provided by Wildlife Research – Franz Suchentrunk.

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Authors and Affiliations

  1. Laboratory of Functional Physiology and Valorization of Bioresources, Higher Institute of Biotechnology of Béja, University of Jendouba, Béja, 9000, Tunisia

    A. Awadi & H. Ben Slimen

  2. Research Institute of Wildlife Ecology, University of Veterinary Medicine Vienna, Savoyenstrasse 1, Vienna, 1160, Austria

    S. Smith & F. Suchentrunk

  3. Faculty of Sciences of Tunis, LR01ES05 Biochimie et Biotechnologie, University of Tunis El Manar, Tunis, 2092, Tunisia

    M. Makni

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  1. A. Awadi
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Correspondence to H. Ben Slimen.

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Awadi, A., Ben Slimen, H., Smith, S. et al. Patterns of evolution in MHC class II DQA and DQB exon 2 genes of Alpine mountain hares, Lepus timidus varronis, and sympatric and parapatric brown hares, L. europaeus, from Switzerland. Immunogenetics 76, 37–50 (2024). https://doi.org/10.1007/s00251-023-01328-2

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