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

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          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.

          Abstract

          Host-parasite coevolution can lead to arms races favouring novel immunogenetic alleles or the maintenance of diversity in a balanced polymorphism. Here, Lighten et al. combine data on MHC diversity across three guppy species and simulations to show that polymorphisms of immunogenetic supertypes may persist even as alleles within supertypes are involved in an arms race.

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          A new evolutionary law

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            Whole-genome duplication in teleost fishes and its evolutionary consequences.

            Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change.
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              MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years?

              Elucidating how natural selection promotes local adaptation in interaction with migration, genetic drift and mutation is a central aim of evolutionary biology. While several conceptual and practical limitations are still restraining our ability to study these processes at the DNA level, genes of the major histocompatibility complex (MHC) offer several assets that make them unique candidates for this purpose. Yet, it is unclear what general conclusions can be drawn after 15 years of empirical research that documented MHC diversity in the wild. The general objective of this review is to complement earlier literature syntheses on this topic by focusing on MHC studies other than humans and mice. This review first revealed a strong taxonomic bias, whereby many more studies of MHC diversity in natural populations have dealt with mammals than all other vertebrate classes combined. Secondly, it confirmed that positive selection has a determinant role in shaping patterns of nucleotide diversity in MHC genes in all vertebrates studied. Yet, future tests of positive selection would greatly benefit from making better use of the increasing number of models potentially offering more statistical rigour and higher resolution in detecting the effect and form of selection. Thirdly, studies that compared patterns of MHC diversity within and among natural populations with neutral expectations have reported higher population differentiation at MHC than expected either under neutrality or simple models of balancing selection. Fourthly, several studies showed that MHC-dependent mate preference and kin recognition may provide selective factors maintaining polymorphism in wild outbred populations. However, they also showed that such reproductive mechanisms are complex and context-based. Fifthly, several studies provided evidence that MHC may significantly influence fitness, either by affecting reproductive success or progeny survival to pathogens infections. Overall, the evidence is compelling that the MHC currently represents the best system available in vertebrates to investigate how natural selection can promote local adaptation at the gene level despite the counteracting actions of migration and genetic drift. We conclude this review by proposing several directions where future research is needed.
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                Author and article information

                Contributors
                Jackielighten@gmail.com
                c.van-oosterhout@uea.ac.uk
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                3 November 2017
                3 November 2017
                2017
                : 8
                : 1294
                Affiliations
                [1 ]ISNI 0000 0001 1092 7967, GRID grid.8273.e, School of Environmental Sciences, , University of East Anglia, ; Norwich, Norfolk NR4 7TJ UK
                [2 ]ISNI 0000000118820937, GRID grid.7362.0, Molecular Ecology and Fisheries Genetics Laboratory, Environment Centre Wales, School of Biological Sciences, , Bangor University, ; Bangor, LL57 2UW UK
                [3 ]GRID grid.430529.9, Department of Life Sciences, , The University of the West Indies, ; St Augustine, Trinidad and Tobago
                [4 ]GRID grid.420132.6, Earlham Institute, , Norwich Research Park Innovation Centre, ; Colney Lane, Norwich NR4 7UZ UK
                [5 ]ISNI 0000 0004 1936 8200, GRID grid.55602.34, Marine Gene Probe Laboratory, Department of Biology, , Dalhousie University, ; 1355 Oxford Street, Halifax, NS Canada B3H 4R2
                [6 ]ISNI 0000 0001 2288 9830, GRID grid.17091.3e, Michael Smith Laboratories, , University of British Columbia, ; 2185 East Mall, Vancouver, BC Canada V6T 1Z4
                [7 ]Science Branch, Department of Fisheries and Oceans Canada, 80 East White Hills Road, St. John’s, NL Canada A1C 5X1
                [8 ]ISNI 0000 0004 1936 8649, GRID grid.14709.3b, McGill University, ; 859 Sherbrooke Street West, Montreal, QC Canada H3A 0C4
                [9 ]ISNI 0000 0004 1936 8649, GRID grid.14709.3b, Redpath Museum, , McGill University, ; 859 Sherbrooke Street West, Montreal, QC Canada H3A 0C4
                Author information
                http://orcid.org/0000-0001-6589-754X
                Article
                1183
                10.1038/s41467-017-01183-2
                5670221
                29101318
                698310a2-4fe7-4b46-b549-8cfc92b55fda
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 February 2017
                : 23 August 2017
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