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

Jackie Lighten; Alexander S.T. Papadopulos; Ryan S. Mohammed; Ben J. Ward; G. Ian Paterson; Lyndsey Baillie; Ian R. Bradbury; Andrew P. Hendry; Paul Bentzen; Cock Van Oosterhout

doi:10.1038/s41467-017-01183-2

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

Jackie Lighten, Alexander S.T. Papadopulos, Ryan S. Mohammed, Ben J. Ward, G. Ian Paterson, Lyndsey Baillie, Ian R. Bradbury, Andrew P. Hendry, Paul Bentzen, Cock Van Oosterhout

Research output: Contribution to journal › Article › peer-review

52 Citations (Scopus)

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.

Original language	English
Article number	1294
Journal	Nature Communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-01183-2
Publication status	Published - Dec 1 2017

Bibliographical note

Funding Information:
This research was funded by a British Ecological Society Large Research Grant (5875–6919) awarded to J.L., a Special Research Opportunity Grant (356373-07) from the Natural Sciences and Engineering Research Council of Canada (NSERC) awarded to A.H. and P.B., a NSERC Discovery Grant (249682-12) to P.B., and grants from The Leverhulme Trust (RPG-2013-305) and Biotechnology and Biological Sciences Research Council (BBSRC) (BB/N02317X/1) awarded to C.v.O., as well as support by the Earth & Life Systems Alliance (ELSA). The authors thank Karl Phillips for helpful comments on an earlier version of the manuscript.

Publisher Copyright:
© 2017 The Author(s).

ASJC Scopus Subject Areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General Physics and Astronomy

PubMed: MeSH publication types

Journal Article
Research Support, Non-U.S. Gov't

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10.1038/s41467-017-01183-2

Cite this

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title = "Evolutionary genetics of immunological supertypes reveals two faces of the Red Queen",

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.",

author = "Jackie Lighten and Papadopulos, {Alexander S.T.} and Mohammed, {Ryan S.} and Ward, {Ben J.} and Paterson, {G. Ian} and Lyndsey Baillie and Bradbury, {Ian R.} and Hendry, {Andrew P.} and Paul Bentzen and {Van Oosterhout}, Cock",

note = "Funding Information: This research was funded by a British Ecological Society Large Research Grant (5875–6919) awarded to J.L., a Special Research Opportunity Grant (356373-07) from the Natural Sciences and Engineering Research Council of Canada (NSERC) awarded to A.H. and P.B., a NSERC Discovery Grant (249682-12) to P.B., and grants from The Leverhulme Trust (RPG-2013-305) and Biotechnology and Biological Sciences Research Council (BBSRC) (BB/N02317X/1) awarded to C.v.O., as well as support by the Earth & Life Systems Alliance (ELSA). The authors thank Karl Phillips for helpful comments on an earlier version of the manuscript. Publisher Copyright: {\textcopyright} 2017 The Author(s).",

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

Abstract

Bibliographical note

ASJC Scopus Subject Areas

PubMed: MeSH publication types

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