Abstract
The adaptive immune system has long been considered a key evolutionary innovation of the vertebrates, the product of two rounds of genome duplication that gave rise to the raw material necessary for the evolution of a highly specific immune response and immune memory. While comparative studies of a small number of model organisms have led to the commonly held view that the adaptive immune system has remained relatively static since its origin, recent studies of non-model organisms are challenging this notion, highlighting the fact that we have only begun to scratch the surface in terms of our understanding of immune system diversity. Some of the most exciting recent results have come from the comparative analysis of teleost fishes, a group that includes more than 40% of vertebrates, and shows remarkable diversity in immune system structure and function. Despite the repeated loss of key components of the adaptive immune machinery in this group, affected species are capable of mounting a robust response to immune challenge, suggesting that they have evolved alternative mechanisms of immune protection. Such deviations from the canonical model of vertebrate immunity create opportunities to explore common paradigms of immune function, and may contribute to new experimental approaches and methods of treatment.
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References
Ackerman AL, Cresswell P (2004) Cellular mechanisms governing cross-presentation of exogenous antigens. Nat Immunol 5:678–684. doi:10.1038/ni1082
Ahmed R, Gray D (1996) Immunological memory and protective immunity: understanding their relation. Science 272:54–60. doi:10.1126/science.272.5258.54
Alejo A, Tafalla C (2011) Chemokines in teleost fish species. Dev Comp Immunol 35:1215–1222. doi:10.1016/j.dci.2011.03.011
Bahr A, Wilson AB (2012) The evolution of MHC diversity: evidence of intralocus gene conversion and recombination in a single-locus system. Gene 497:52–57. doi:10.1016/j.gene.2012.01.017
Bahr A, Sommer S, Mattle B, Wilson AB (2012) Mutual mate choice in the potbellied seahorse (Hippocampus abdominalis). Behav Ecol 23:869–878. doi:10.1093/beheco/ars045
Barber LD, Parham P (1993) Peptide binding to major histocompatibility complex molecules. Ann Rev Cell Biol 9:163–206. doi:10.1146/annurev.cb.09.110193.001115
Barrangou R, Marraffini LA (2014) CRISPR-CAS systems: prokaryotes upgrade to adaptive immunity. Mol Cell 54:234–244. doi:10.1016/j.molcel.2014.03.011
Basta S, Alatery A (2007) The cross-priming pathway: a portrait of an intricate immune system. Scand J Immunol 65:311–319. doi:10.1111/j.1365-3083.2007.01909.x
Beemelmanns A, Roth O (2017) Grandparental immune priming in the pipefish Syngnathus typhle. BMC Evol Biol 17:44. doi:10.1186/s12862-017-0885-3
Birrer SC, Reusch TBH, Roth O (2012) Salinity change impairs pipefish immune defence. Fish Shellfish Immunol 33:1238–1248. doi:10.1016/j.fsi.2012.08.028
Boehm T (2011) Design principles of adaptive immune systems. Nat Rev Immunol 11:307–317
Cooper MD, Herrin BR (2010) How did our complex immune system evolve? Nat Rev Immunol 10:2–3. doi:10.1038/nri2686
Datta SK, Redecke V, Prilliman KR et al (2003) A subset of toll-like receptor ligands induces cross-presentation by bone marrow-derived dendritic cells. J Immunol 170:4102–4110
Dijkstra JM, Grimholt U, Leong J et al (2013) Comprehensive analysis of MHC class II genes in teleost fish genomes reveals dispensability of the peptide-loading DM system in a large part of vertebrates. BMC Evol Biol 13:260. doi:10.1186/1471-2148-13-260
Flajnik MF, Kasahara M (2009) Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet 11:47–59
Flajnik MF, Deschacht N, Muyldermans S (2011) A case of convergence: why did a simple alternative to canonical antibodies arise in sharks and camels? PLoS Biol 9:e1001120
Froese R, Pauly D (2010) FishBase. In: www.fishbase.org. http://www.fishbase.org
Grimholt U (2016) MHC and evolution in teleosts. Biology (Basel). doi: 10.3390/biology5010006
Grimholt U, Larsen S, Nordmo R et al (2003) MHC polymorphism and disease resistance in Atlantic salmon (Salmo salar); facing pathogens with single expressed major histocompatibility class I and class II loci. Immunogenetics 55:210–219. doi:10.1007/s00251-003-0567-8
Grimholt U, Tsukamoto K, Azuma T et al (2015) A comprehensive analysis of teleost MHC class I sequences. BMC Evol Biol 15:32. doi:10.1186/s12862-015-0309-1
Haase D, Roth O, Kalbe M et al (2013) Absence of major histocompatibility complex class II mediated immunity in pipefish, Syngnathus typhle: evidence from deep transcriptome sequencing. Biol Lett 9:20130044. doi:10.1098/rsbl.2013.0044
Herrin BR, Cooper MD (2010) Alternative adaptive immunity in jawless vertebrates. J Immunol 185:1367–1374
Hsu E, Pulham N, Rumfelt LL, Flajnik MF (2006) The plasticity of immunoglobulin gene systems in evolution. Immunol Rev 210:8–26
Hughes AL (2007) Looking for Darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 99:364–373
Hughes AL, Nei M (1989) Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6:559–579. doi:10.1093/oxfordjournals.molbev.a040573
Kasahara M (1997) New insights into the genomic organization and origin of the major histocompatibility complex: role of chromosomal (genome) duplication in the emergence of the adaptive immune system. Hereditas 127:59–65. doi:10.1111/j.1601-5223.1997.t01-1-00059.x
Kaufman J, Salomonsen J, Flajnik M (1994) Evolutionary conservation of MHC class I and class II molecules—different yet the same. Semin Immunol 6:411–424
Kelley J, Walter L, Trowsdale J (2005) Comparative genomics of major histocompatibility complexes. Immunogenetics 56:683–695
Kurtz J, Armitage SA (2006) Alternative adaptive immunity in invertebrates. Trends Immunol 27:493–496
Lin Q, Fan S, Zhang Y et al (2016) The seahorse genome and the evolution of its specialized morphology. Nature 540:395–399. doi:10.1038/nature20595
Magnadóttir B (1998) Comparison of immunoglobulin (IgM) from four fish species. Icel Agr Sci 12:47–59
Malmstrøm M, Jentoft S, Gregers TF, Jakobsen KS (2013) Unraveling the evolution of the Atlantic cods (Gadus morhua L.) alternative immune strategy. PLoS One 8:e74004. doi:10.1371/journal.pone.0074004
Malmstrøm M, Matschiner M, Tørresen OK et al (2016) Evolution of the immune system influences speciation rates in teleost fishes. Nat Genet 48:1204–1210. doi:10.1038/ng.3645
Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945. doi:10.1002/bies.20293
Mikkelsen H, Lund V, Larsen R, Seppola M (2011) Vibriosis vaccines based on various sero-subgroups of Vibrio anguillarum O2 induce specific protection in Atlantic cod (Gadus morhua L.) juveniles. Fish Shellfish Immunol 30:330–339. doi:10.1016/j.fsi.2010.11.007
Near TJ, Eytan RI, Dornburg A et al (2012) Resolution of ray-finned fish phylogeny and timing of diversification. Proc Natl Acad Sci U S A 109:13698–13703. doi:10.1073/pnas.1206625109
Nei M, Gu X, Sitnikova T (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system. Proc Natl Acad Sci U S a 94:7799–7806
Ohno S (1970) Evolution by Gene duplication. Springer Science & Business Media, New York
Palti Y (2011) Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol 35:1263–1272. doi:10.1016/j.dci.2011.03.006
Palti Y, Rodriguez MF, Gahr SA, Hansen JD (2007) Evolutionary history of the ABCB2 genomic region in teleosts. Dev Comp Immunol 31:483–498
Pilström L, Warr GW, Strömberg S (2005) Why is the antibody response of Atlantic cod so poor? The search for a genetic explanation. Fish Sci 71:961–971. doi:10.1111/j.1444-2906.2005.01052.x
Reche PA, Reinherz EL (2003) Sequence variability analysis of human class I and class II MHC molecules: functional and structural correlates of amino acid polymorphisms. J Mol Biol 331:623–641
Rocha N, Neefjes J (2008) MHC class II molecules on the move for successful antigen presentation. EMBO J 27:1–5. doi:10.1038/sj.emboj.7601945
Rölle A, Pollmann J, Cerwenka A (2013) Memory of infections: an emerging role for natural killer cells. PLoS Pathog 9:e1003548. doi:10.1371/journal.ppat.1003548
Rønneseth A, Wergeland HI, Pettersen EF (2007) Neutrophils and B-cells in Atlantic cod (Gadus morhua L.) Fish Shellfish Immunol 23:493–503. doi:10.1016/j.fsi.2006.08.017
Roth O, Keller I, Landis SH et al (2012a) Hosts are ahead in a marine host–parasite coevolutionary arms race: innate immune system adaptation in pipefish Syngnathus typhle against Vibrio phylotypes. Evolution 66:2528–2539. doi:10.1111/j.1558-5646.2012.01614.x
Roth O, Klein V, Beemelmanns A et al (2012b) Male pregnancy and biparental immune priming. Am Nat 180:802–814. doi:10.1086/668081
Santini F, Harmon LJ, Carnevale G, Alfaro ME (2009) Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evol Biol 9:194. doi:10.1186/1471-2148-9-194
Schluter SF, Bernstein RM, Bernstein H, Marchalonis JJ (1999) Big Bang emergence of the combinatorial immune system. Dev Comp Immunol 23:107–111. doi:10.1016/S0145-305X(99)00002-6
Secombes CJ, Wang T, Bird S (2011) The interleukins of fish. Dev Comp Immunol 35:1336–1345. doi:10.1016/j.dci.2011.05.001
Small CM, Bassham S, Catchen J et al (2016) The genome of the Gulf pipefish enables understanding of evolutionary innovations. Genome Biol 17:258. doi:10.1186/s13059-016-1126-6
Snell GD (1948) Methods for the study of histocompatibility genes. J Genet 49:87–108
Star B, Jentoft S (2012) Why does the immune system of Atlantic cod lack MHC II? BioEssays 34:648–651. doi:10.1002/bies.201200005
Star B, Nederbragt AJ, Jentoft S et al (2011) The genome sequence of Atlantic cod reveals a unique immune system. Nature 477:207–210
Stet RJM, Kruiswijk CP, Dixon B (2003) Major histocompatibility lineages and immune gene function in teleost fishes: the road not taken. Crit Rev Immunol 23:441–471
Sundaram AY, Kiron V, Dopazo J, Fernandes JM (2012) Diversification of the expanded teleost-specific toll-like receptor family in Atlantic cod, Gadus morhua. BMC Evol Biol 12:256. doi:10.1186/1471-2148-12-256
Sunyer JO (2013) Fishing for mammalian paradigms in the teleost immune system. Nat Immunol 14:320–326. doi:10.1038/ni.2549
Sunyer JO, Boshra H, Lorenzo G et al (2003) Evolution of complement as an effector system in innate and adaptive immunity. Immunol Res 27:549–564. doi:10.1385/IR:27:2-3:549
Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Ann Rev Genet 38:615–643. doi:10.1146/annurev.genet.38.072902.092831
Uribe C, Folch H, Enriquez R, Moran G (2011) Innate and adaptive immunity in teleost fish: a review. Vet Med 56:486–503
Wedekind C, Walker M, Portmann J et al (2004) MHC-linked susceptibility to a bacterial infection, but no MHC-linked cryptic female choice in whitefish. J Evol Biol 17:11–18. doi:10.1046/j.1420-9101.2004.00669.x
Wilson AB, Whittington CM, Bahr A (2014) High intralocus variability and interlocus recombination promote immunological diversity in a minimal major histocompatibility system. BMC Evol Biol 14:273. doi:10.1186/s12862-014-0273-1
Acknowledgements
I am grateful to Martin Flajnik, Unni Grimholt, and Oriol Sunyer for illuminating discussions on the incredible diversity of vertebrate immunity.
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This article is published in the Special Issue MHC Genes and Their Ligands in Health and Disease with Editor Prof. Ronald Bontrop.
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Wilson, A.B. MHC and adaptive immunity in teleost fishes. Immunogenetics 69, 521–528 (2017). https://doi.org/10.1007/s00251-017-1009-3
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DOI: https://doi.org/10.1007/s00251-017-1009-3