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Immunological MHC supertypes and allelic expression: how low is the functional MHC diversity in free-ranging Namibian cheetahs?

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Abstract

Cheetahs (Acinonyx jubatus) are a textbook example of how habitat loss, human-wildlife conflicts and historic bottlenecks depleted genetic variability, both genome-wide and at the major histocompatibility complex (MHC), which plays an integral role in the adaptive immune response. However, free-ranging Namibian cheetahs show no signs of impaired immunocompetence or health. This contradicts theoretical expectations and poses the question whether the manner by which MHC diversity is judged needs to be revised. Here, we show that free-ranging Namibian cheetahs still harbour MHC alleles that are divergent enough to cover several functionally distinct MHC supertypes and thus are probably capable of binding and presenting a relatively broad range of antigens to T-cells. We detected a similar pattern in three other free-ranging, strongly bottlenecked cat species, supporting the hypothesis that species with a low MHC allelic diversity might be able to retain functional diversity not within but across loci. Moreover, the allelic composition influences the level of MHC class I and class II expression which also might play a significant role in pathogen defence. Thus, our study indicates that the evolutionary role of MHC diversity goes beyond counting the remaining number of MHC alleles and offers an explanation as to how cat species might have avoided impaired immuno-competence, despite showing low MHC allelic diversity. Although the low MHC diversity currently seems to be sufficient to ensure the health of free-ranging cheetahs, it is currently unknown whether it can provide sufficient protection from future threats through emerging new pathogens.

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Acknowledgements

We thank the German Research Foundation (DFG; SO 428/10-1), the Leibniz Institute for Zoo and Wildlife Research (IZW) in Germany and the Messerli Foundation in Switzerland for funding this study. We also thank the Namibian Ministry of Environment and Tourism for permission to conduct the research, the Namibian farmers for their support and collaboration and the team members of the IZW cheetah research project, especially Jörg Melzheimer and Annika Weigold, for valuable assistance in the field. We are grateful to Anke Schmidt for providing help in the laboratory and Theresa Jones for language editing. Two anonymous reviewers provided very useful comments on a former draft of this manuscript.

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Schwensow, N., Castro-Prieto, A., Wachter, B. et al. Immunological MHC supertypes and allelic expression: how low is the functional MHC diversity in free-ranging Namibian cheetahs?. Conserv Genet 20, 65–80 (2019). https://doi.org/10.1007/s10592-019-01143-x

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