Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen

Jackie Lighten (), Alexander S. T. Papadopulos, Ryan S. Mohammed, Ben J. Ward, Ian Paterson, Lyndsey Baillie, Ian R. Bradbury, Andrew P. Hendry, Paul Bentzen and Cock van Oosterhout ()
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Jackie Lighten: University of East Anglia
Alexander S. T. Papadopulos: Bangor University
Ryan S. Mohammed: The University of the West Indies
Ben J. Ward: Norwich Research Park Innovation Centre
Ian Paterson: Dalhousie University
Lyndsey Baillie: University of British Columbia
Ian R. Bradbury: Dalhousie University
Andrew P. Hendry: McGill University
Paul Bentzen: Dalhousie University
Cock van Oosterhout: University of East Anglia

Nature Communications, 2017, vol. 8, issue 1, 1-11

Abstract: Abstract Red Queen host–parasite co-evolution can drive adaptations of immune genes by positive selection that erodes genetic variation (Red Queen arms race) or results in a balanced polymorphism (Red Queen dynamics) and long-term preservation of genetic variation (trans-species polymorphism). These two Red Queen processes are opposite extremes of the co-evolutionary spectrum. Here we show that both Red Queen processes can operate simultaneously by analysing the major histocompatibility complex (MHC) in guppies (Poecilia reticulata and P. obscura) and swamp guppies (Micropoecilia picta). Sub-functionalisation of MHC alleles into ‘supertypes’ explains how polymorphisms persist during rapid host–parasite co-evolution. Simulations show the maintenance of supertypes as balanced polymorphisms, consistent with Red Queen dynamics, whereas alleles within supertypes are subject to positive selection in a Red Queen arms race. Building on the divergent allele advantage hypothesis, we show that functional aspects of allelic diversity help to elucidate the evolution of polymorphic genes involved in Red Queen co-evolution.

Date: 2017
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DOI: 10.1038/s41467-017-01183-2

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