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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.

SUBMITTER: Lighten J

PROVIDER: S-EPMC5670221 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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

Lighten Jackie J Papadopulos Alexander S T AST Mohammed Ryan S RS Ward Ben J BJ G Paterson Ian I Baillie Lyndsey L Bradbury Ian R IR Hendry Andrew P AP Bentzen Paul P van Oosterhout Cock C

Nature communications 20171103 1

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 ...[more]

PMID: 29101318

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Project description:BACKGROUND:Red Queen dynamics are defined as long term co-evolutionary dynamics, often with oscillations of genotype abundances driven by fluctuating selection in host-parasite systems. Much of our current understanding of these dynamics is based on theoretical concepts explored in mathematical models that are mostly (i) deterministic, inferring an infinite population size and (ii) evolutionary, thus ecological interactions that change population sizes are excluded. Here, we recall the different mathematical approaches used in the current literature on Red Queen dynamics. We then compare models from game theory (evo) and classical theoretical ecology models (eco-evo), that are all derived from individual interactions and are thus intrinsically stochastic. We assess the influence of this stochasticity through the time to the first loss of a genotype within a host or parasite population. RESULTS:The time until the first genotype is lost ("extinction time"), is shorter when ecological dynamics, in the form of a changing population size, is considered. Furthermore, when individuals compete only locally with other individuals extinction is even faster. On the other hand, evolutionary models with a fixed population size and competition on the scale of the whole population prolong extinction and therefore stabilise the oscillations. The stabilising properties of intra-specific competitions become stronger when population size is increased and the deterministic part of the dynamics gain influence. In general, the loss of genotype diversity can be counteracted with mutations (or recombination), which then allow the populations to recurrently undergo negative frequency-dependent selection dynamics and selective sweeps. CONCLUSION:Although the models we investigated are equal in their biological motivation and interpretation, they have diverging mathematical properties both in the derived deterministic dynamics and the derived stochastic dynamics. We find that models that do not consider intraspecific competition and that include ecological dynamics by letting the population size vary, lose genotypes - and thus Red Queen oscillations - faster than models with competition and a fixed population size.

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

Publications

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

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