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

Nature Communications
Jackie LightenCock van Oosterhout

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.

References

Jan 1, 1990·Immunologic Research·E K WakelandW K Potts
Apr 1, 1990·Proceedings of the National Academy of Sciences of the United States of America·N Takahata
Jul 22, 1997·Proceedings of the National Academy of Sciences of the United States of America·M NeiT Sitnikova
Dec 21, 2000·Molecular Ecology·A Richman
Nov 29, 2002·Nature Genetics·Mark E J WoolhouseBruce R Levin
Sep 25, 2003·Evolution; International Journal of Organic Evolution·Daniel Garrigan, Philip W Hedrick
Nov 26, 2003·Journal of Evolutionary Biology·L Bernatchez, C Landry
Jan 22, 2004·Bioinformatics·Emmanuel ParadisKorbinian Strimmer
Mar 3, 2004·Proceedings of the National Academy of Sciences of the United States of America·Andres AguilarRobert K Wayne
Mar 23, 2004·The Journal of Immunology : Official Journal of the American Association of Immunologists·Irini A DoytchinovaDarren R Flower
Jan 24, 2007·Bioinformatics·Tomer Hertz, Chen Yanover
Apr 27, 2007·Proceedings of the National Academy of Sciences of the United States of America·Mario ReckerSunetra Gupta
Dec 14, 2007·Annual Review of Genetics·Jan KleinNikolas Nikolaidis
Jan 24, 2008·BMC Immunology·John SidneyAlessandro Sette
Aug 23, 2008·Journal of Evolutionary Biology·S GandonT Day
Nov 7, 2008·Proceedings. Biological Sciences·Cock van Oosterhout
Feb 25, 2009·Molecular Ecology·Lou Jost
Sep 4, 2009·Genetica·Bonnie A Fraser, Bryan D Neff
Dec 24, 2009·Immunology·Derek Middleton, Faviel Gonzelez
Jan 15, 2010·Proceedings. Biological Sciences·Lewis G Spurgin, David S Richardson
Feb 10, 2012·Molecular Biology and Evolution·V LlaurensC van Oosterhout
Jun 24, 2014·Molecular Ecology·Jackie LightenPaul Bentzen

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Citations

Jan 18, 2018·Proceedings of the National Academy of Sciences of the United States of America·Karl P PhillipsJacek Radwan
Jun 13, 2018·Molecular Biology and Evolution·Federica Pierini, Tobias L Lenz
Mar 7, 2019·Royal Society Open Science·Elizabeth L Anzia, Jomar F Rabajante
Sep 29, 2020·Heredity·Magdalena Herdegen-RadwanJacek Radwan
Jun 29, 2018·G3 : Genes - Genomes - Genetics·Débora Y C BrandtDiogo Meyer
Oct 21, 2018·Nature Communications·Maciej J EjsmondJacek Radwan
May 18, 2019·Molecular Ecology·Roberta BergeroDeborah Charlesworth
Feb 2, 2020·Parasitology Research·Jakub Vlček, Jan Štefka
Mar 29, 2020·Royal Society Open Science·Ryan S MohammedJackie Lighten
Dec 5, 2020·Molecular Ecology·Willow SmallboneJoanne Cable
Feb 12, 2020·Trends in Genetics : TIG·Jacek RadwanJamie Winternitz
Aug 10, 2021·Evolution; International Journal of Organic Evolution·Timothy K O'ConnorNoah K Whiteman
Jan 15, 2022·Journal of Evolutionary Biology·Lydia J Buckingham, Ben Ashby

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Methods Mentioned

BETA
PCR
genotyping
electrophoresis
PCRs

Software Mentioned

Micro
MEGA
Minitab
R
FIGTREE
ape package
SPADE R package
LOSITAN
adagenet
Checker

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