Abstract
Immunity mechanisms have existed since early life forms arose around 3700 million years ago (MYA) but the sophistication and complexity of reactions towards invasive molecules and organisms has increased immensely since. The Cambrian explosion around 500 MYA was associated with a rich expansion of life forms and species and with this event appeared a plethora of immune gene and protein variations. In general, the main pillars of immunity cover (1) recognition of self/non-self; (2) immunological memory; (3) cell-to-cell signaling; (4) humoral effector mechanisms; and (5) cellular effector mechanisms. The cellular arm of immunity is a basic requirement present in early amoebae that allowed them to demonstrate phagocytosis and extracellular trapping of pathogens. Unicellular organisms, such as ciliates, are also able to differentiate self from non-self. Immunological memory, involving cellular and humoral factors, can be traced in invertebrates, such as snails, providing the host organism with lasting protection against invading pathogens. Innate immunological reactions comprising both cellular and humoral factors have in this way proven protective for invertebrates, but with the advent of vertebrates the adaptive branch of immunity became highly developed, involving variable lymphocyte receptors and major histocompatibility complex (MHC). Teleost fishes display in principle a well-developed immune system dependent on myeloid and lymphoid cell lines, immunological memory, immunoglobulin production, MHC, and antigen presentation. Signal molecules orchestrating complex immune reactions can be traced in rather early invertebrates, but the richness and diversity of cytokine families appeared with fishes. The adaptive features have a close connection with the innate immune mechanisms that have in modern times developed into the armament protecting amphibians, reptiles, birds, and mammals from adverse molecules and pathogens.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abelli L (2016) Developmental biology of teleost lymphocytes. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 215–226
Arizza V, Schillaci D (2016) Echinoderm antimicrobial peptides: the ancient arms of the deuterostome innate immune system. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 159–176
Bartl S, Nonaka M (2015) MHC molecules of cartilaginous fishes. In: Smith SL, Sim RB, Flajnik MF (eds) Immunobiology of the shark. CRC Press – Taylor & Francis, Boca Raton, USA
Baxter RHG, Contet A, Krueger K (2017) Arthropod innate immune systems and vector-borne diseases. Biochemistry 56:907–918
Berrien-Elliott MM, Wagner JA, Fehniger TA (2015) Human cytokine-induced memory like natural killer cells. J Innate Immun 7:563–571
Betti M, Ciacci C, Lorusso LC, Canonico B, Falcioni T, Gallo G, Canesi L (2006) Effects of tumour necrosis factor alpha (TNFLx) on Mytilus haemocytes: role of stress-activated mitogen-activated protein kinases (MAPKs). Biol Cell 98:233–244. https://doi.org/10.1242/BC20050049
Bilej M, De Baetselier P, Beschin A (2000) Antimicrobial defense of the earthworm. Folia Microbiol 45(4):283–300. https://doi.org/10.1007/BF02817549
Boudinot P, Zou J, Ota T, Buonocore F, Scapigliati G, Canapa G, Cannon J, Litman G, Hansen JD (2014) A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths. J Exp Zool (Mol Dev Evol) 9999B:1–23. https://doi.org/10.1002/jez.b.22559
Buchmann K (2014) Evolution of innate immunity: clues from invertebrates via fish to mammals. Front Immunol 5:1–8. https://doi.org/10.3389/fimmu.2014.00459
Cammarata M, Parisi MG, Vasta GR (2016) Evolution and immune function of fish lectins. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 239–256
Canesi L, Pruzzo C (2016) Specificity of innate immunity in bivalves: a lesson from bacteria. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier – Academic Press, London. ISBN 978-0-12-803252-7, pp 79–92
Cerenius L, Söderhäll K (2004) The prophenoloxidase activating system in invertebrates. Immunol Rev 198:116–126
Chettri JK, Holten-Andersen L, Raida MK, Kania P, Buchmann K (2011) PAMP induced expression of immune relevant genes in head kidney leukocytes of rainbow trout (Oncorhynchus mykiss). Dev Comp Immunol 35:476–482. https://doi.org/10.1016/j.dci.2010.12001
Chettri JK, Kuhn JA, Jaafar RM, Kania PW, Møller OS, Buchmann K (2014) Epidermal response of rainbow trout to Ichthyobodo necator: immunohistochemical and gene expression studies indicate a Th1/Th2-like switch. J Fish Dis. https://doi.org/10.1111/jfd.12169
Clark SE, Eichelberger KR, Weiser JN (2013) Evasion of killing by human antibody and complement through multiple variations in the surface oligosaccharide of Haemophilus influenzae. Mol Microbiol 88:603–618. https://doi.org/10.1111/mmi.12214
Cooper EL (1968) Transplantation immunity in annelids. I. Rejection of xenografts exchanged between Lumbricus terrestris and Eisenia foetida. Transplantation 6:322–337
Cooper EL (1969) Chronic allograft rejection in Lumbricus terrestris. J Exp Zool 171:69–73
Cooper EL (2010) Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys Life Rev 7:55–78. https://doi.org/10.1016/j.plrev.2009.12.001
Coscia MR, Giacomelli S, Oreste U (2016) Teleost immunoglobulins. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 257–274
Cytrynska M, Wojda I, Jakubowicz T (2016) How insects combat infections. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 117–128
Danchin EG, Abi-Rached L, Gilles A, Pontarotti P (2003) Conservation of the MHC-like region throughout evolution. Immunogenetics 55:141–148
Desjardins M, Houde M, Gagnon E (2005) Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol Rev 207:158–167. https://doi.org/10.1111/j.0105-2896.2005.00319.x
Detournay O, Schnitzler CE, Poole A, Weis VM (2012) Regulation of cnidarian-dinoflagellate mutualisms: evidence that activation of a host TGF beta innate immune pathway promotes tolerance to the symbiont. Dev Comp Immunol 38(4):525–537. https://doi.org/10.1016/j.dci.2012.08.008
Dishaw LJ, Litman GW (2009) Invertebrate allorecognition: the origins of histocompatibility. Curr Biol 19(7):R286–R288. https://doi.org/10.1093/bfg.els007
Dunin-Horkawicz S, Klaus KO, Lupas AN (2014) Procaryotic protein networks mediating innate immunity and apoptosis. J Mol Biol 426:1568–1582. https://doi.org/10.1016/j.jmb.2013.11.030
Dzik JM (2010) The ancestry and cumulative evolution of immune reactions. Acta Biochim Pol 57:443–466
Elvitigala DAS, Premachandra HKA, Whang I, Nam B-H, Lee J (2013) Molecular insights of the first gastropod TLR counterpart from disk abalone (Haliotis discus discus) revealing its transcriptional modulation under pathogenic stress. Fish Shellfish Immunol 35:334–342. https://doi.org/10.1016/fsi.2013.04.031
Engelmann P, Hayashi Y, Bodo K, Molnar L (2016) New aspects of earthworm innate immunity: novel molecules and old proteins with unexpected functions. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 53–66
Franchi N, Ballarin L (2016) Cytotoxic cells of compound ascidians. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 193–204
Franzenburg S, Fraune S, Kunzel S, Baines JF, Domazet-Loso T, Bosch TCG (2012) My D88-deficient Hydra reveal an ancient function of TLR signaling in sensing in sensing bacterial colonizers. Proc Natl Acad Sci U S A 109(47):19374–19379. https://doi.org/10.1073/pnas.1213110109
Fujito NT, Sugimoto S, Nonaka M (2010) Evolution of thioester containing proteins revealed by cloning and characterization of their genes from a cnidarian sea anemone, Haliplanella lineate. Dev Comp Immunol 34:775–784. https://doi.org/10.1016/j.dci.2010.02011
Fuller- Espie SL (2010) Vertebrate cytokines interleukin12 and gamma interferon, but not interleukin 10, enhance phagocytosis in the annelid Eisenia hortensis. J Invertebr Pathol 104:119–124. https://doi.org/10.1016/j.pp.2010.02.009
Gao Z, Li M, Ma J, Zhang SC (2014) An Amphioxus gC1q protein binds human IgG and initiates the classical pathway: implications for a C1q-mediated complement system in the basal chordate. Eur J Immunol 44(12):3680–3695
Garcia AB, Pierce RJ, Gourbal B, Werkmeister E, Colinet D, Reichart JM, Dissous C, Coustau C (2010) Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog 6:e1001115. https://doi.org/10.1371/journal.ppat.1001115
Gosh J, Lun CM, Majeske AJ, Sacchi S, Schrankel CS, Smith LC (2011) Invertebrate immune diversity. Dev Comp Immunol 35:959–974. https://doi.org/10.1016/j.dci.2010.12.009
Hahn UK, Bender RC, Bayne CJ (2000) Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev Comp Immunol 24:531–541. https://doi.org/10.1016/S0145-305x(00)00017-3
Hahn UK, Bender RC, Bayne CJ (2001) Involvement of nitric oxide in killing Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J Parasitol 87(4):778–785. https://doi.org/10.1645/0022-3395(2001)087
Hassenkam T, Andersson MP, Dalby KN, Mackenzie DMA, Rosing MT (2017) Elements of Eoarchean life trapped in mineral inclusions. Nature 0:1–15. https://doi.org/10.1038/nature23261
Hauton C (2012) The scope of the crustacean immune system for disease control. J Invertebr Pathol 110:251–260. https://doi.org/10.1016/j.jip.2012.03.005
Héja D, Kocsics A, Dobo J, Szilagyi K, Szasz R, Zavodszky P, Pal G, Gal P (2012) Revised mechanism of complement lectin-pathway activation revealing the role of serine protease MASP-1 as the exclusive activator of MASP-2. Proc Natl Acad Sci U S A 109(26):10498–10503
Jin P, Hu J, Qian JJ, Chen LM, Xu XF, Ma F (2012) Identification and characterization of a putative lipopolysaccharide-induced TNF-alpha factor (LITAF) gene from Amphioxus (Branchiostoma belcheri): an insight into the innate immunity of Amphioxus and the evolution of LITAF. Fish Shellfish Immunol 32:1223–1228. https://doi.org/10.1016/j.fsi.2012.03.030
Kaiser P (2010) Advances in avian immunology – prospects for disease control: a review. Avian Pathol 39(5):309–324. https://doi.org/10.1080/03079457.2010.508777
Kasahara M, Suzuki T, Du Pasquier L (2004) On the origins of the adaptive immune system: novel insights from invertebrates and cold-blooded vertebrates. Trends Immunol 25(2):105–111. https://doi.org/10.1016/j.it.2003.11.005
Kishishita N, Nagawa F (2014) Evolution of adaptive immunity: implications of a third lymphocyte lineage in lampreys. BioEssays 36:244–250. https://doi.org/10.1002/bies.201300145
Kulski JK, Shiina T, Anzai T, Kohara S, Inoko H (2002) Comparative genomic analysis of the MHC: the evolution of class I duplication blocks, diversity and complexity from shark to man. Immunol Rev 190(1):95–122. https://doi.org/10.1034/j.1600-065x.2002.19008.x
Lin XH, Söderhäll I (2011) Crustacean hematopoiesis and the astakine cytokines. Blood 117:6417–6424. https://doi.org/10.1182/blood-2010-11320614
Lin L, Zhang JQ (2017) Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol 18:2. https://doi.org/10.1186/s12865-016-0187-3
Lin XH, Novotny M, Söderhäll K, Söderhäll I (2010) Ancient cytokines, the role of astakines as hematopoietic growth factors. J Biol Chem 285:28577–28586. https://doi.org/10.1074/jbc.M110.138560
Litman GW, Rast JP, Fugmann SD (2010) The origins of vertebrate adaptive immunity. Nat Rev Immunol 10:543–553. https://doi.org/10.1038/nri2807
Malagoli D, Sacchi S, Ottaviandi E (2008) Unpaired (upd)-3 expression and other immune-related functions are stimulated by interleukin-8 in Drosophila melanogaster SL2 cell line. Cytokine 44:269–274. https://doi.org/10.1016/j.cyto.2008.08.011
Meng FY, Mai KS, Ma HM, Zhang WB (2009) The evolution of echinoderm immunology. Prog Biochem Biophys 36(7):803–809. https://doi.org/10.3724/SP.J.1206.2008.00761
Mills CD (2012) M1 and M2 macrophages: oracles of health and disease. Crit Rev Immunol 32(06):463–488
Mills CD, Ley K, Buchmann K, Canton J (2015) Sequential immune responses: the weapons of immunity. J Innate Immun 7:443–449. https://doi.org/10.1159/000380910
Nicola F, Loriano B (2017) Morula cells as key hemocytes of the lectin pathway of complement activation in the colonial tunicate Botryllus schlosseri. Fish Shellfish Immunol 63:157–164
Nicolo P, Matteo C, Daniela P, Aiti V (2016) Inflammatory response of the ascidian Ciona intestinalis. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 177–192
Nonaka M, Yoshizaki F (2004) Primitive complement system of invertebrates. Immunol Rev 198:203–215. https://doi.org/10.1111/j.0105-2896.2004.00118.x
Peiser L, Mukhopadhyay S, Gordon S (2002) Scavenger receptors in innate immunity. Curr Opin Immunol 14:123–128. https://doi.org/10.1016/S0952-7915(01)00307-7
Peng MX, Niu DH, Wang F, Chen ZY, Li J (2016) Complement C3 gene: expression characterization and innate immune response in razor clam Sinonovacula constricta. Fish Shellfish Immunol 55:223–232
Perovic-Ottstadt S, Adell T, Proksch P, Wiens M, Korshev M, Gamulin V, Müller IM, Müller WE (2004) A (1-3) beta recognition protein from the sponge Suberites domuncula. Mediated activation of fibrinogen related protein and epidermal growth factor gene expression. Eur J Biochem 271:1924–1937. https://doi.org/10.1111/j.1432-1033.2004.04102.x
Pinaud S, Portela J, Duval D, Nowacki FC et al (2016) A shift from cellular to humoral responses contributes innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1005361
Rhodes CP, Ratcliffe NA, Rowley AF (1982) Presence of coelomocytes in the primitive chordate Amphioxus (Branchiostoma lanceolatum). Science 217:263–265. https://doi.org/10.1126/science.7089565
Roberts S, Gueguen Y, de Lorgeril J, Goetz F (2008) Rapid accumulation of an interleukin 17 homolog transcript in Crassostrea gigas hemocytes following bacterial exposure. Dev Comp Immunol 32(9):1099–1104. https://doi.org/10.1016/j.dci.2008.02.006
Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillasmury C (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329:1353–1355
Roth O, Kurtz J (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scabe (Crustacea: Isopoda). Dev Comp Immunol 33(11):1151–1155
Salazar-Jaramillo L, Paspati A, Van de Zande L, Vermeulen CJ, Schwander T, Wertheim B (2014) Evolution of a cellular immune response in Drosophila: a phenotypic and genomic comparative analysis. Genome Biol Evol 6:273–289
Schmid-Hempel P (2009) Immune defence, parasite evasion strategies and their relevance for macroscopic phenomena such as virulence. Philos Trans R Soc 364:85–98. https://doi.org/10.1098/rstb.2008.0157
Schonhofer C, Coatsworth H, Caicedo P, Ocampo C, Lowenberger C (2016) Aedes aegypti immune responses to Dengue virus. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 129–144
Scocchi M, Furlan M, Venier P, Pallavicini A (2016) Cathelicidins: an ancient family of fish antimicrobial peptides. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 227–238
Secombes CJ, Zou J (2017) Evolution of interferons and interferon receptors. Front Immunol 8:1–10. https://doi.org/10.3389/fimmu.2017.00209
Skanta F, Roubalova R, Dvorak J, Prochazkova P, Bilej M (2013) Molecular cloning and expression of TLR in the Eisenia and rei earthworm. Dev Comp Immunol 41(4):694–702. https://doi.org/10.1016/j.dci.2013.08.009
Suurväli J, Jouneau L, Thépot D, Grusea S, Pontarotti P, Pasquier LD, Boudinot SR, Boudinot P (2014) The proto-MHC of placozoans, a region specialized in cellular stress and ubiquitination (proteasome pathways). J Immunol. https://doi.org/10.4049/jimmunol.1401177
Vallesi A, Alimenti C, Luporini P (2016) Ciliate pheromones: primordial self−/nonself-recognition signals. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 1–16
Venier P, Domeneghetti S, Sharma N, Pallavivini A, Gerdol M (2016) Immune related signaling in mussel and bivalves. In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 93–106
Venkatesh B, Lee AP, Ravi V et al (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505:174–179. https://doi.org/10.1038/nature12826
Vizioli J, Drago F, Lefebvre C (2016) Neuroprotection and immunity in the medicinal leech Hirudo medicinalis: what about microglia? In: Ballarin L, Cammarata M (eds) Lessons in immunity – from single cell organisms to mammals. Elsevier –Academic Press, London. ISBN 978-0-12-803252-7, pp 64–78
Wang T, Secombes CJ (2013) The cytokine networks of adaptive immunity in fish. Fish Shellfish Immunol 35:1703–1718. https://doi.org/10.1016/j.fsi.2013.08.030
Watthanasororut A, Söderhäll K, Jiravanichpaisal P, Söderhäll I (2011) An ancient cytokine, astakine, mediates circadian regulation of invertebrate hematopoiesis. Cell Mol Life Sci 68(2):315–323. https://doi.org/10.1007/s00018-010-0458-8
Yuen B, Bayes JM, Degnan SM (2013) The characterization of sponge NLRs provides insight into the origin and evolution of this innate immune gene family in animals. Mol Biol Evol 31:106–120. https://doi.org/10.1093/molbev/mst174
Zeng DG, Lei AY, Chen XH (2013) Cloning, characterization and expression of the macrophage migration inhibitory factor gene from Pacific white shrimp Litopenaeus vannamei (Penaeidae). Genet Mol Res 12:5872–5879. https://doi.org/10.4238/2013.November.22.15
Zhang Y-A, Salinas I, Li J, Parra D, Bjork S, Xu Z, LaPatra S, Bartholomew J, Sunyer JO (2010a) IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat Immunol 11:827–836. https://doi.org/10.1038/ni.1913
Zhang Y, Zhao JM, Zhang H, Gai YC, Wang LL, Li FM, Yang JL, Qiu LM, Song LS (2010b) The involvement of suppressors of cytokine signaling 2 (SOCS2) in immune defense responses of Chinese mitten crab Eriocheir sinensis. Dev Comp Immunol 34:42–48. https://doi.org/10.1016/j.dci.2009.08.001
Zhang Y, Li J, Yu F, He XC, Yu ZN (2013) Allograft inflammatory factor-1 stimulates hemocyte immune activation by enhancing phagocytosis and expression of inflammatory cytokines in Crassostrea gigas. Fish Shellfish Immunol 34:1071–1077. https://doi.org/10.1016/j.fsi.2013.01.014
Zhang YN, Xu K, Deng AQ, Fu X, Xu AL, Liu X (2014) An Amphioxus RAG1-like DNA fragment encodes a functional central domain of vertebrate core RAG1. Proc Natl Acad Sci U S A 11:397–402. https://doi.org/10.1073/pnas.1318843111
Zhang X, Zhuchenko O, Kuspa A, Soldati T (2015) Social amoebae trap and kill bacteria by casting DNA nets. Nat Commun 7:10938. https://doi.org/10.1038/ncomms10938. (1-9)
Zhou L, Zhang LH, Camara M, He YW (2017) The DSF family of quorum sensing signals: diversity, biosynthesis and turnover. Trends Microbiol 25(4):293–303. https://doi.org/10.1016/j.tim.2016.11.013
Zimmerman LM, Vogel LA, Bowden RM (2010) Understanding the vertebrate immune system: insights from the reptilian perspective. J Exp Biol 213:661–671. https://doi.org/10.1242/jeb.038315
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Buchmann, K. (2018). Evolution of Immunity. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_1
Download citation
DOI: https://doi.org/10.1007/978-3-319-76768-0_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-76767-3
Online ISBN: 978-3-319-76768-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)