in

Diversity of MHC IIB genes and parasitism in hybrids of evolutionarily divergent cyprinoid species indicate heterosis advantage

  • 1.

    Arnold, M. L. Natural Hybridization and Evolution (Oxford University Press, 1997).

    Google Scholar 

  • 2.

    Stelkens, R. & Seehausen, O. Genetic distance between species predicts novel trait expression in their hybrids. Evolution 63, 884–897 (2009).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 3.

    Grant, P. R. & Grant, B. R. Hybridization of bird species. Science 256, 193–197 (1992).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 4.

    Saino, N. & Villa, S. Pair composition and reproductive success across a hybrid zone of carrion crows and hooded crows. Auk 109, 543–555 (1992).

    Google Scholar 

  • 5.

    Good, T. P., Ellis, J. C., Annett, C. A. & Pierotti, R. Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution 54, 1774–1783 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 6.

    Bartley, D. M., Rana, K. & Immink, A. J. The use of inter-specific hybrids in aquaculture and fisheries. Rev. Fish Biol. Fisher. 10, 325–337 (2001).

    Article 

    Google Scholar 

  • 7.

    Rosenfield, J. A., Nolasco, S., Lindauer, S., Sandoval, C. & Kodric-Brown, A. The role of hybrid vigor in the replacement of Pecos pupfish by its hybrids with sheepshead minnow. Conserv. Biol. 18, 1589–1598 (2004).

    Article 

    Google Scholar 

  • 8.

    Sun, Y. et al. Comparative transcriptomic study of muscle provides new insights into the growth superiority of a novel grouper hybrid. PLoS ONE 11, e0168802 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 9.

    Scribner, K. T., Page, K. S. & Bartron, M. L. Hybridization in freshwater fishes: A review of case studies and cytonuclear methods of biological inference. Rev. Fish Biol. Fisher. 10, 293–323 (2001).

    Article 

    Google Scholar 

  • 10.

    Ottová, E. et al. Evolution and trans-species polymorphism of MHC class IIB genes in cyprinid fish. Fish Shellfish Immun. 18, 199–222 (2005).

    Article 
    CAS 

    Google Scholar 

  • 11.

    Šimková, A. et al. Does invasive Chondrostoma nasus shift the parasite community structure of endemic Parachondrostoma toxostoma in sympatric zones?. Parasite. Vector. 5, 200 (2012).

    Article 

    Google Scholar 

  • 12.

    Klein, J. & OhUigin, C. MHC polymorphism and parasites. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346, 351–358 (1994).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 13.

    Klein, J., Klein, D., Figueroa, F., OhUigin, C. & Sato, A. Major histocompatibility complex genes in the study of fish phylogeny. In Molecular Systematic of Fishes (eds Kocher, T. D. & Stepien, C. A.) 271–283 (Academic Press, 1997).

    Chapter 

    Google Scholar 

  • 14.

    Hughes, A. L. & Nei, M. Nucleotide substitution at major histocompatibility complex class II loci: Evidence for overdominant selection. Proc. Nat. Acad. Sci. USA 56, 958–962 (1989).

    ADS 
    Article 

    Google Scholar 

  • 15.

    Klein, J. & OhUigin, C. Composite origin of major histocompatibility complex genes. Curr. Opin. Genet. Dev. 3, 923–930 (1993).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 16.

    Hughes, A. L. & Nei, M. Models of host-parasite interactions and MHC polymorphism. Genetics 132, 863–864 (1992).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 17.

    Klein, J. Of HLA, tryps, and selection? An essay on coevolution of MHC and parasites. Hum. Immunol. 30, 247–258 (1991).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 18.

    Hughes, A. L., Hughes, M. K., Howell, C. Y. & Nei, M. Natural selection at the class II major histocompatibility complex loci of mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 346, 359–367 (1994).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 19.

    Hedrick, P. W. Pathogen resistence and genetic variation at MHC loci. Evolution 56, 1902–1908 (2002).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 20.

    Nowak, M. A., Tarczy-Hornoch, K. & Austyn, J. M. The optimal number of major histocompatibility complex molecules in an individual. Proc. Nat. Acad. Sci. U.S.A. 89, 10896–10899 (1992).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 21.

    Wegner, K. M., Reusch, T. B. H. & Kalbe, M. Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J. Evol. Biol. 16, 224–232 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 22.

    Eizaguirre, C., Lenz, T. L., Traulsen, A. & Milinski, M. Speciation accelerated and stabilized by pleiotropic major histocompatibility complex immunogenes. Ecol. Lett. 12, 5–12 (2009).

    PubMed 
    Article 

    Google Scholar 

  • 23.

    Nadachowska-Brzyska, K., Zielinski, P., Radwan, J. & Babiks, W. Interspecific hybridization increases MHC class II diversity in two sister species of newts. Mol. Ecol. 21, 887–906 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 24.

    Wegner, K. M. & Eizaguirre, C. New(t)s and views from hybridizing MHC genes: Introgression rather than trans-species polymorphism may shape allelic repertoires. Mol. Ecol. 21, 779–781 (2012).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 25.

    Dudek, K., Gaczorek, T. S., Zielinski, P. & Babik, W. Massive introgression of major histocompatibility complex (MHC) genes in newt hybrid zones. Mol. Ecol. 28, 4798–4810 (2019).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 26.

    Šimková, A., Civáňová, K., Gettová, L. & Gilles, A. Genomic porosity between invasive Chondrostoma nasus and endangered endemic Parachondrostoma toxostoma (Cyprinidae): The evolution of MHC IIB genes. PLoS ONE 8, e65883 (2013).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 27.

    Zhang, S., Wang, Z. & Wang, H. Maternal immunity in fish. Dev. Comp. Immunol. 39, 72–78 (2013).

    ADS 
    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 28.

    Šimková, A., Vojtek, L., Halačka, K., Hyršl, P. & Vetešník, L. The effect of hybridization on fish physiology, immunity and blood biochemistry: A case study in hybridizing Cyprinus carpio and Carassius gibelio (Cyprinidae). Aquaculture 435, 381–389 (2015).

    Article 
    CAS 

    Google Scholar 

  • 29.

    Cowx, I. G. The biology of bream, Abramis brama (L), and its natural hybrid with roach, Rutilus rutilus (L), in the River Exe. J. Fish Biol. 22, 631–646 (1983).

    Article 

    Google Scholar 

  • 30.

    Economidis, P. S. & Wheeler, A. Hybrids of Abramis brama with Scardinius erythrophthalmus and Rutilus rutilus from Lake Volvi, Macedonia, Greece. J. Fish Biol. 35, 295–299 (1989).

    Article 

    Google Scholar 

  • 31.

    Toscano, B. J. et al. An ecomorphological framework for the coexistence of two cyprinid fish and their hybrids in a novel environment. Biol. J. Linn. Soc. 99, 768–783 (2010).

    Article 

    Google Scholar 

  • 32.

    Hayden, B. et al. Hybridisation between two cyprinid fishes in a novel habitat: Genetics, morphology and life-history traits. BMC Evol. Biol. 10, 169 (2010).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 33.

    Kuparinen, A., Vinni, M., Teacher, A. G. F., Kähkönen, K. & Merilä, J. Mechanism of hybridization between bream Abramis brama and roach Rutilus rutilus in their native range. J. Fish Biol. 84, 237–242 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 34.

    Konopinski, M. K. & Amirowicz, A. Genetic composition of a population of natural common bream Abramis brama x roach Rutilus rutilus hybrids and their morphological characteristics in comparison with parent species. J. Fish Biol. 92, 365–385 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 35.

    Krasnovyd, V., Vetešník, L., Gettová, L., Civáňová, K. & Šimková, A. Patterns of parasite distribution in the hybrids of non-congeneric cyprinid fish species: Is asymmetry in parasite infection the result of limited coadaptation?. Int. J. Parasitol. 47, 471–483 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 36.

    Hayden, B. et al. Trophic dynamics within a hybrid zone—interactions between an abundant cyprinid hybrid and sympatric parental species. Freshwater Biol. 56, 1723–1735 (2011).

    Article 

    Google Scholar 

  • 37.

    Nzau Matondo, B. et al. Hybridization success of three common European cyprinid species, Rutilus rutilus, Blicca bjoerkna and Abramis brama and larval resistance to stress tests. Fish. Sci. 73, 1137–1146 (2007).

    Article 
    CAS 

    Google Scholar 

  • 38.

    Hayden, B., McLoone, P., Coyne, J. & Caffrey, J. M. Extensive hybridization between roach, Rutilus rutilus L., and common bream, Abramis brama L. Irish lakes and rivers. Biol. Environ. 114B, 35–39 (2014).

    Google Scholar 

  • 39.

    Eizaguirre, C. et al. Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging threespined stickleback ecotypes. Evol. Ecol. 25, 605–622 (2011).

    Article 

    Google Scholar 

  • 40.

    Hubbs, C. L. Hybridization between fish species in nature. Syst. Zool. 4, 1–20 (1955).

    Article 

    Google Scholar 

  • 41.

    Rauch, G., Kalbe, M. & Reusch, T. B. H. Relative importance of MHC and genetic background for parasite load in a field experiment. Evol. Ecol. Res. 8, 373–386 (2006).

    Google Scholar 

  • 42.

    Eizaguirre, C., Lenz, T. L., Kalbe, M. & Milinski, M. Divergent selection on locally adapted major histocompatibility complex immune genes experimentally proven in the field. Ecol. Lett. 15, 723–731 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 43.

    Šimková, A., Dávidová, M., Papoušek, I. & Vetešník, L. Does interspecies hybridization affect the host specificity of parasites in cyprinid fish?. Parasite. Vector. 6, 95 (2013).

    Article 

    Google Scholar 

  • 44.

    Seifertová, M., Jarkovský, J. & Šimková, A. Does the parasite-mediated selection drive the MHC class IIB diversity in wild populations of European chub (Squalius cephalus)?. Parasitol. Res. 115, 1401–1415 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 45.

    Nzau Matondo, B., Ovidio, M., Philippart, J. C. & Poncin, P. Reproductive behaviour and sexual production in the first-generation hybrids of roach Rutilus rutilus L. × common bream Abramis brama L. J. Appl. Ichthyol. 27, 859–867 (2011).

    Article 

    Google Scholar 

  • 46.

    Graser, R., OhUigin, C., Vincek, V., Meyer, A. & Klein, J. Trans-species polymorphism of class II Mhc loci in danio fishes. Immunogenetics 44, 36–48 (1996).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 47.

    Figueroa, F. et al. MHC class IIB gene evolution in East African cichlid fishes. Immunogenetics 51, 556–575 (2000).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 48.

    Migalska, M., Sebastian, A. & Radwan, J. Major histocompatibility complex class I diversity limits the repertoire of T cell
    receptors.Proc. Natl. Acad. Sci. USA 116, 5021–5026 (2019).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 49.

    Šimková, A., Košař, M., Vetešník, L. & Vyskočilová, M. MHC genes and parasitism in Carassius gibelio, a diploid-triploid fish species with dual reproduction strategies. BMC Evol. Biol. 13, 122 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 50.

    Borghans, J. A. M., Beltman, J. B. & De Boer, J. B. MHC polymorphism under host-pathogen coevolution. Immunogenetics 55, 732–739 (2004).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 51.

    Ejsmond, M. J. & Radwan, J. Red queen processes drive positive selection on major histocompatibility complex (MHC) genes. PLoS Comput. Biol. 11, e1004627 (2015).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 52.

    Phillips, K. P. et al. Immunogenetic novelty confers a selective advantage in host-pathogen coevolution. Proc. Natl. Acad. Sci. USA 115, 1552–1557 (2018).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 53.

    Gaigher, A., Burri, R., San-Jose, L. M., Roulin, A. & Fumagalli, L. Lack of statistical power as a major limitation in understanding MHC-mediated immunocompetence in wild vertebrate populations. Mol. Ecol. 28, 5115–5132 (2019).

    PubMed 
    Article 

    Google Scholar 

  • 54.

    Šimková, A., Ottová, E. & Morand, S. MHC variability, life-traits and parasite diversity of European cyprinid fish. Evol. Ecol. 20, 465–477 (2006).

    Article 

    Google Scholar 

  • 55.

    Clarke, B. & Kirby, D. R. S. Maintenance of histocompatibility polymorphisms. Nature 211, 999–1000 (1966).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 56.

    Meglécz, E. et al. SESAME (SEquence Sorter & AMplicon Explorer): Genotyping based on high throughput multiplex amplicon sequencing. Bioinformatics 27, 277–278 (2011).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • 57.

    Zagalska-Neubauer, M. et al. 454 sequencing reveals extreme complexity of the class II major histocompatibility complex in the collared flycatcher. BMC Evol. Biol. 10, 395 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 58.

    Van Erp, S. H. M., Egberts, E. & Stet, R. J. M. Characterization of class II A and B genes in a gynogenetic carp clone. Immunogenetics 44, 192–202 (1996).

    PubMed 
    Article 

    Google Scholar 

  • 59.

    Šimková, A. Major histocompatibility complex genes and parasites in cyprinid fish. Vie Milieu 67, 139–148 (2017).

    Google Scholar 

  • 60.

    Klein, J. et al. Nomenclature for the major histocompatibility complexes of different species: A proposal. Immunogenetics 31, 217–219 (1990).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 61.

    Dixon, B., Nagelkerke, L. A. J., Sibbing, F. A., Egberts, E. & Stet, R. J. M. Evolution of MHC class II beta chain-encoding genes in the Lake Tana barbel species flock (Barbus intermedius complex). Immunogenetics 44, 419–431 (1996).

    CAS 
    PubMed 

    Google Scholar 

  • 62.

    Rakus, K. L. et al. Major histocompatibility (MH) class IIB gene polymorphism influences disease resistance of common carp (Cyprinus carpio L). Aquaculture 288, 44–50 (2009).

    CAS 
    Article 

    Google Scholar 

  • 63.

    Seifertová, M. & Šimková, A. Structure, diversity and evolutionary patterns of expressed MHC class IIB genes in chub (Squalius cephalus), a cyprinid fish species from Europe. Immunogenetics 63, 167–181 (2011).

    PubMed 
    Article 

    Google Scholar 

  • 64.

    Ronquist, F. et al. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across large model space. Syst. Biol. 61, 539–542 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 65.

    Darriba, D., Taboala, G. L., Doallo, R. & Posada, D. J. ModelTest2: More models, new heuristics and parallel computing. Nat. Methods 9, 772 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 66.

    Yang, Z. H. PAML4: Phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 67.

    Doledec, S. & Chessel, D. Co-inertia analysis—an alternative method for studying species environment relationships. Freshwater Biol. 31, 277–294 (1994).

    Article 

    Google Scholar 

  • 68.

    Dray, S., Chessel, D. & Thioulouse, J. Co-inertia analysis and the linking of ecological data tables. Ecology 84, 3078–3089 (2003).

    Article 

    Google Scholar 

  • 69.

    Deter, J. et al. Association between the DQA MHC class II gene and puumala virus infection in Myodes glareolus, the bank vole. Infect. Genet. Evol. 8, 450–458 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • 70.

    Evans, M. L. & Neff, B. D. Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha). Mol. Ecol. 18, 4716–4729 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 71.

    Zuur, A. et al. Mixed Effects Models and Extensions in Ecology With R (Springer, 2009).

    MATH 
    Book 

    Google Scholar 

  • 72.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach 2nd edn. (Springer, 2002).

    MATH 

    Google Scholar 

  • 73.

    R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/(2018).

  • 74.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article 

    Google Scholar 

  • 75.

    Bartoń, K. MuMIn: Multi-Model Inference. R package version 1.15.1. http://CRAN.R-project.org/package=MuMIn (2018).

  • 76.

    Thioulouse, J. & Dray, S. Interactive multivariate data analysis in R with the ade4 and ade4tkgui packages. J. Stat. Softw. 22, 1–14 (2007).

    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Correction: Divergence of a genomic island leads to the evolution of melanization in a halophyte root fungus

    A peculiar state of matter in layers of semiconductors