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Molluscan Immunobiology: Challenges in the Anthropocene Epoch

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Advances in Comparative Immunology

Abstract

The Mollusca, with a long and rich evolutionary history, is one of the most speciose and distinctive of the animal phyla. Among its members are some of the largest and most long-lived, intelligent, and commercially valuable invertebrate species, contributing massively to the human food supply. Some are valued for their beauty, and others are significant disease vectors. In this chapter, after first providing an overview of the diverse and often distinctive infectious agents with which molluscs must contend, we outline in broad strokes some of the major features of molluscan immune systems. Molluscs continue to enrich our broader understanding of immunology, both from a steady stream of new insights in genomic and postgenomic studies and from novel discoveries such as transmissible neoplasia, which challenge our understanding of cancer and basic processes such as allorecognition. We then discuss how the rapidly changing modern world often exposes molluscs to significant abiotic and biotic challenges—often presented in daunting combinations—that elicit complex responses and reveal the extent to which stress and immune responses are intertwined. We conclude with a discussion of aspects of molluscan immunobiology about which we need to expand our scope of knowledge if molluscs are not to suffer more than they already have in this, the world’s sixth major episode of mass extinction.

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References

  • Adema CM (2015) Fibrinogen-related proteins (FREPs) in mollusks. In: Hsu E, DuPasquier L (eds) Pathogen-host interactions: antigenic variation v. somatic adaptations. Results Probl Cell Differ, vol 57. Springer, Cham, pp 111–129

    Google Scholar 

  • Adema CM, Loker ES (1997) Specificity and immunobiology of larval digenean–snail associations. In: Fried B, Graczyk TK (eds) Advances in trematode biology. CRC Press, Boca Raton, pp 229–263

    Google Scholar 

  • Adema CM, Loker ES (2015) Digenean–gastropod host associations inform on aspects of specific immunity in snails. Dev Comp Immunol 48(2):275–283

    CAS  PubMed  Google Scholar 

  • Adema CM, Van Deutekom-Mulder EC, Van der Knaap WPW et al (1993) NADPH-oxidase activity: the probable source of reactive oxygen intermediate generation in hemocytes of the gastropod Lymnaea-stagnalis. J Leukoc Biol 54(5):379–383

    CAS  PubMed  Google Scholar 

  • Adema CM, Arguello DF, Stricker SA et al (1994) A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa. J Parasitol 80(5):719–727

    CAS  PubMed  Google Scholar 

  • Adema CM, Hertel LA, Miller RD et al (1997) A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci U S A 94(16):8691–8696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Adema CM, Hanington PC, Lun C-M et al (2010) Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes). Mol Immunol 47(4):849–860

    CAS  PubMed  Google Scholar 

  • Adema CM, Bayne CJ, Bridger JM et al (2012) Will all scientists working on snails and the diseases they transmit please stand up? PLoS Negl Trop Dis 6(12):e1835

    PubMed  PubMed Central  Google Scholar 

  • Adema CM, Hillier LW, Jones CS, Loker ES et al (2017) Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nat Commun 16(8):15451

    Google Scholar 

  • Allam B, Espinosa EP (2016) Bivalve immunity and response to infections: are we looking at the right place? Fish Shellfish Immunol 53:4–12

    CAS  PubMed  Google Scholar 

  • Allam B, Raftos D (2015) Immune responses to infectious diseases in bivalves. J Invertebr Pathol 131:121–136

    CAS  PubMed  Google Scholar 

  • Allam B, Paillard C, Ford SE (2002) Pathogenicity of Vibrio tapetis, the etiological agent of brown ring disease in clams. Dis Aquat Org 48(3):221–231

    Google Scholar 

  • Allam B, Espinosa EP, Tanguy A et al (2014) Transcriptional changes in Manila clam (Ruditapes philippinarum) in response to brown ring disease. Fish Shellfish Immunol 41(1):2–11

    CAS  PubMed  Google Scholar 

  • Allan ERO, Tennessen JA, Bollmann SR et al (2017) Schistosome infectivity in the snail, Biomphalaria glabrata, is partially dependent on the expression of Grctm6, a Guadeloupe resistance complex protein. PLoS Negl Trop Dis 11(2):e0005362

    PubMed  PubMed Central  Google Scholar 

  • Allegretti SM, Carvalho JF, Magalhaes LA et al (2009) Behaviour of albino and melanic variants of Biomphalaria glabrata Say, 1818 (Mollusca: Planorbidae) following infection by Schistosoma mansoni Sambon, 1907. Braz J Biol 69(1):217–222

    CAS  PubMed  Google Scholar 

  • Alphey L (2016) Can CRISPR-Cas9 gene drives curb malaria? Nat Biotechnol 34(2):149–150

    CAS  PubMed  Google Scholar 

  • Amen RI, Baggen JM, Meuleman EA et al (1991) Trichobilharzia ocellata: quantification of effects on haemocytes of the pond snail Lymnaea stagnalis by morphometric means. Tissue Cell 23(5):665–676

    CAS  PubMed  Google Scholar 

  • Anderson RS (1977) Biochemistry and physiology of invertebrate macrophages in vitro. In: Bulla LA, Cheng TC (eds) Comparative pathobiology, vol vol 3. Springer, Boston

    Google Scholar 

  • Arzul I, Carnegie RB (2015) New perspective on the haplosporidian parasites of molluscs. J Invertebr Pathol 131:32–42

    PubMed  Google Scholar 

  • Arzul I, Nicolas JL, Davison AJ et al (2001) French scallops: a new host for ostreid herpesvirus-1. Virology 290(2):342–349

    CAS  PubMed  Google Scholar 

  • Aschtgen M-S, Lynch JB, Koch E et al (2016) Rotation of Vibrio fischeri flagella produces outer membrane vesicles that induce host development. J Bacteriol 198(16):2156–2165

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asplund ME, Baden SP, Russ S et al (2014) Ocean acidification and host–pathogen interactions: blue mussels, Mytilus edulis, encountering Vibrio tubiashii. Environ Microbiol 16(4):1029–1039

    PubMed  Google Scholar 

  • Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6(10):973–979

    CAS  PubMed  Google Scholar 

  • Baeza Garcia A, Pierce RJ, Gourbal B et al (2010) Involvement of the cytokine MIF in the snail host immune response to the parasite Schistosoma mansoni. PLoS Pathog 6(9):e1001115

    PubMed  PubMed Central  Google Scholar 

  • Barbosa L, Caldeira RL, Carvalho OS et al (2006) Resistance to Schistosoma mansoni by transplantation of APO Biomphalaria tenagophila. Parasite Immunol 28(5):209–212

    CAS  PubMed  Google Scholar 

  • Baron OL, van West P, Industri B et al (2013) Parental transfer of the antimicrobial protein LBP/BPI protects Biomphalaria glabrata eggs against oomycete infections. PLoS Pathog 9(12):e1003792

    PubMed  PubMed Central  Google Scholar 

  • Baron OL, Deleury E, Reichhart J-M et al (2016) The LBP/BPI multigenic family in invertebrates: evolutionary history and evidences of specialization in mollusks. Dev Comp Immunol 57:20–30

    CAS  PubMed  Google Scholar 

  • Bayne CJ (1998) Invertebrate cell culture considerations: insects, ticks, shellfish, and worms (Review). In: Methods in cell biology, vol 57. Academic Press, New York, pp 187–201

    Google Scholar 

  • Bayne CJ (2009) Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165(1):8–18

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bayne B (2017) Biology of oysters, vol 41. Academic Press, New York

    Google Scholar 

  • Beaudry A, Fortier M, Masson S et al (2016) Effect of temperature on immunocompetence of the blue mussel (Mytilus edulis). J Xenobiot 6(1):8–13

    CAS  Google Scholar 

  • Bender RC, Bayne CJ (1996) Purification and characterization of a tetrameric alpha-macroglobulin proteinase inhibitor from the gastropod mollusc Biomphalaria glabrata. Biochem J 316(Pt 3):893–900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bender RC, Fryer SE, Bayne CJ (1992) Proteinase inhibitory activity in the plasma of a mollusc: evidence for the presence of alpha-macroglobulin in Biomphalaria glabrata. Comp Biochem Physiol B. 102(4):821–824

    CAS  Google Scholar 

  • Bender RC, Bixler LM, Lerner JR et al (2002) Schistosoma mansoni sporocysts in culture: host plasma hemoglobin contributes to in vitro oxidative stress. J Parasitol 88(1):14–18

    CAS  PubMed  Google Scholar 

  • Bender RC, Broderick EJ, Goodall CP et al (2005) Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni–resistant snails produce more extracellular H2O2 than susceptible snails. J Parasitol 91(2):275–279

    CAS  PubMed  Google Scholar 

  • Bender RC, Goodall CP, Blouin MS et al (2007) Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosoma mansoni. Dev Comp Immunol 31(9):874–878

    CAS  PubMed  Google Scholar 

  • Betcher MA, Fung JM, Han AW et al (2012) Microbial distribution and abundance in the digestive system of five shipworm species (Bivalvia: Teredinidae). PLoS One 7(9):e45309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Blaise C, Trottier S, Gagne F et al. (2002) Immunocompetence of bivalve hemocytes as evaluated by a miniaturized phagocytosis assay. Environ Toxicol 17(3):160–169

    CAS  PubMed  Google Scholar 

  • Boisseaux P, Noury P, Thomas H et al (2017) Immune responses in the aquatic gastropod Lymnaea stagnalis under short-term exposure to pharmaceuticals of concern for immune systems: diclofenac, cyclophosphamide and cyclosporine A. Ecotoxicol Environ Saf 139:358–366

    CAS  PubMed  Google Scholar 

  • Bouchut A, Roger E, Coustau C et al (2006) Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 36(2):175–184

    CAS  PubMed  Google Scholar 

  • Boyd WC, Brown R, Boyd LG (1966) Agglutinins for human erythrocytes in mollusks. J Immunol 96(2):301–303

    CAS  PubMed  Google Scholar 

  • Buckley KM, Rast JP (2015) Diversity of animal immune receptors and the origins of recognition complexity in the deuterostomes. Dev Comp Immunol 49(1):179–189

    CAS  PubMed  Google Scholar 

  • Buddenborg SK, Bu L, Zhang S-M et al (2017) Transcriptomic responses of Biomphalaria pfeifferi to Schistosoma mansoni: investigation of a neglected African snail that supports more S. mansoni transmission than any other snail species. PLoS Negl Trop Dis 11:e0005984

    PubMed  PubMed Central  Google Scholar 

  • Burioli EAV, Prearo M, Houssin M (2017) Complete genome sequence of Ostreid herpesvirus type 1 μVar isolated during mortality events in the Pacific oyster Crassostrea gigas in France and Ireland. Virology 509:239–251. https://doi.org/10.1016/j.virol.2017.06.027

    Article  CAS  PubMed  Google Scholar 

  • Butler PG (2012) Clam shells, climate change and ageing: the mollusc that had 500 birthdays. Catal Second Sch Rev 23(1):6–8

    Google Scholar 

  • Butt D, Raftos D (2008) Phenoloxidase-associated cellular defence in the Sydney rock oyster, Saccostrea glomerata, provides resistance against QX disease infections. Dev Comp Immunol 32(3):299–306

    CAS  PubMed  Google Scholar 

  • Canesi L, Ciacci C, Bergami E et al (2015) Evidence for immunomodulation and apoptotic processes induced by cationic polystyrene nanoparticles in the hemocytes of the marine bivalve Mytilus. Mar Environ Res 111:34–40

    CAS  PubMed  Google Scholar 

  • Carballal MJ, Barber BJ, Iglesias D et al (2015) Neoplastic diseases of marine bivalves. J Invertebr Pathol 131:83–106

    PubMed  Google Scholar 

  • Carella F, Villari G, Maio N et al (2016) Disease and disorders of freshwater unionid mussels: a brief overview of recent studies. Front Physiol 7:489

    PubMed  PubMed Central  Google Scholar 

  • Carrasco N, Green T, Itoh N (2015) Marteilia spp. parasites in bivalves: a revision of recent studies. J Invertebr Pathol 131:43–57

    PubMed  Google Scholar 

  • Castellanos-Martinez S, Gestal C (2013) Pathogens and immune response of cephalopods. J Exp Mar Biol Ecol 447:14–22

    CAS  Google Scholar 

  • Castellanos-Martinez S, Arteta D, Catarino S et al (2014) De novo transcriptome sequencing of the Octopus vulgaris hemocytes using Illumina RNA-seq technology: response to the infection by the gastrointestinal parasite aggregate octopiana. PLoS One 9(10):e107873. https://doi.org/10.1371/journal.pone.0107873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo MG, Yoshino TP (2002) Carbohydrate inhibition of Biomphalaria glabrata embryonic (Bge) cell adhesion to primary sporocysts of Schistosoma mansoni. Parasitology 125(Pt 6):513–525

    CAS  PubMed  Google Scholar 

  • Castillo MG, Goodson MS, McFall-Ngai M (2009) Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev Comp Immunol 33(1):69–76

    CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo MG, Salazar KA, Joffe NR (2015) The immune response of cephalopods from head to foot. Fish Shellfish Immunol 46(1):145–160

    CAS  PubMed  Google Scholar 

  • Chen JH, Bayne CJ (1995) Bivalve mollusk hemocyte behaviors: characterization of hemocyte aggregation and adhesion and their inhibition in the California mussel (Mytilus californianus). Biol Bull 188(3):255–266

    CAS  PubMed  Google Scholar 

  • Chen G, Zhang C, Jiang F et al (2014) Bioinformatics analysis of hemocyte miRNAs of scallop Chlamys farreri against acute viral necrobiotic virus (AVNV). Fish Shellfish Immunol 37:75–86

    CAS  PubMed  Google Scholar 

  • Cheng TC (1967) Marine molluscs as hosts for symbioses, with a review of known parasites of commercially important species. Adv Mar Biol 5:424

    Google Scholar 

  • Cheng TC, Howland KH (1979) Chemotactic attraction between hemocytes of the oyster, Crassostrea virginica, and bacteria. J Invertebr Pathol 33(2):204–210

    Google Scholar 

  • Ching HL (1991) Lists of larval worms from marine invertebrates of the Pacific Coast of North America. J Helminthol Soc Wash 58(1):57–68

    Google Scholar 

  • Chu H, Mazmanian SK (2013) Innate immune recognition of the microbiota promotes host–microbial symbiosis. Nat Immunol 14(7):668–675

    CAS  PubMed  PubMed Central  Google Scholar 

  • Claes MF (1996) Functional morphology of the white bodies of the cephalopod mollusc Sepia officinalis. Acta Zool 77(2):173–190

    Google Scholar 

  • Coates CJ, Nairn J (2014) Diverse immune functions of hemocyanins. Dev Comp Immunol 45(1):43–55

    CAS  PubMed  Google Scholar 

  • Coleman AW (2000) The significance of a coincidence between evolutionary landmarks found in mating affinity and a DNA sequence. Protist 151(1):1–9

    CAS  PubMed  Google Scholar 

  • Comps M (1988) Epizootic diseases of oysters associated with viral infections. Am Fish Soc Spec Pub 18:23–37

    Google Scholar 

  • Cong M, Song L, Wang L et al (2008) The enhanced immune protection of Zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp Biochem Physiol B Biochem Mol Biol 151(2):191–196

    PubMed  Google Scholar 

  • Corbeil S, Williams LM, McColl KA et al (2016) Australian abalone (Haliotis laevigata, H. rubra and H. conicopora) are susceptible to infection by multiple abalone herpesvirus genotypes. Dis Aquat Org 119(2):101–106

    CAS  Google Scholar 

  • Cosgrove J, McDaniel N (2009) Super suckers, the giant Pacific octopus and other cephalopods of the Pacific Coast. Harbour, British Columbia

    Google Scholar 

  • Cosseau C, Azzi A, Rognon A et al (2010) Epigenetic and phenotypic variability in populations of Schistosoma mansoni: a possible kick-off for adaptive host/parasite evolution. Oikos 119(4):669–678

    CAS  Google Scholar 

  • Costa MM, Novoa B, Figueras A (2008) Influence of beta-glucans on the immune responses of carpet shell clam (Ruditapes decussatus) and Mediterranean mussel (Mytilus galloprovincialis). Fish Shellfish Immunol 24(5):498–505

    Google Scholar 

  • Costa MM, Dios S, Alonso-Gutierrez J et al (2009) Evidence of high individual diversity on myticin C in mussel (Mytilus galloprovincialis). Dev Comp Immunol 33(2):162–170

    CAS  PubMed  Google Scholar 

  • Coustau C, Mitta G, Dissous C et al (2003) Schistosoma mansoni and Echinostoma caproni excretory–secretory products differentially affect gene expression in Biomphalaria glabrata embryonic cells. Parasitology 127(Pt 6):533–542

    CAS  PubMed  Google Scholar 

  • Coustau C, Gourbal B, Duval D et al (2015) Advances in gastropod immunity from the study of the interaction between the snail Biomphalaria glabrata and its parasites: a review of research progress over the last decade. Fish Shellfish Immunol 46(1):5–16

    CAS  PubMed  Google Scholar 

  • Cowie RH, Regnier C, Fontaine B et al (2017) Measuring the sixth extinction: what do mollusks tell us? Nautilus 131(1):3–41

    Google Scholar 

  • Cruz-Flores R, Caceres-Martinez J, Munoz-Flores M et al (2016) Hyperparasitism by the bacteriophage (Caudovirales) infecting Candidatus Xenohaliotis californiensis (Rickettsiales-like prokaryote) parasite of wild abalone Haliotis fulgens and Haliotis corrugata from the Peninsula of Baja California, Mexico. J Invertebr Pathol 140:58–67

    PubMed  Google Scholar 

  • Cunningham AA, Daszak P (1998) Extinction of a species of land snail due to infection with a microsporidian parasite. Conserv Biol 12(5):1139–1141

    Google Scholar 

  • Davies MS, Hawkins SJ (1998) Mucus from marine molluscs. In: Blaxter JHS, Southward AJ, Tyler PA (eds) Advances in marine biology, vol 34. Academic Press/Elsevier Science, London, pp 1–71

    Google Scholar 

  • Davison AJ, Trus BL, Cheng N et al (2005) A novel class of herpesvirus with bivalve hosts. J Gen Virol 86(Pt 1):41–53

    CAS  PubMed  Google Scholar 

  • De Baets K, Klug C, Korn D (2010) Devonian pearls and ammonoid–endoparasite co-evolution. Acta Palaeontol Pol. https://doi.org/10.4202/app.2010.0044

    Google Scholar 

  • De Zoysa M, Whang I, Lee Y et al (2010) Defensin from disk abalone Haliotis discus discus: molecular cloning, sequence characterization and immune response against bacterial infection. Fish Shellfish Immunol 28:261–266

    PubMed  Google Scholar 

  • DeGaffe G, Loker ES (1998) Susceptibility of Biomphalaria glabrata to infection with Echinostoma paraensei: correlation with the effect of parasite secretory–excretory products on host hemocyte spreading. J Invertebr Pathol 71(1):64–72

    CAS  PubMed  Google Scholar 

  • Deleury E, Dubreuil G, Elangovan N et al (2012) Specific versus non-specific immune responses in an invertebrate species: evidenced by a comparative de novo sequencing study. PLoS One 7(3):e32512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Desriac F, Le Chevalier P, Brillet B et al (2014) Exploring the hologenome concept in marine bivalvia: haemolymph microbiota as a pertinent source of probiotics for aquaculture. FEMS Microbiol Lett 350(1):107–116

    CAS  PubMed  Google Scholar 

  • Dheilly NM, Duval D, Mouahid G et al (2015) A family of variable immunoglobulin and lectin domain containing molecules in the snail Biomphalaria glabrata. Dev Comp Immunol 48(1):234–243

    CAS  PubMed  Google Scholar 

  • Distel DL, Altamia MA, Lin Z et al (2017) Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory. Proc Natl Acad Sci U S A 114(18):E3652–E3658

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dmytrenko O, Russell SL, Loo WT et al (2014) The genome of the intracellular bacterium of the coastal bivalve, Solemya velum: a blueprint for thriving in and out of symbiosis. BMC Genomics 15:924

    PubMed  PubMed Central  Google Scholar 

  • Downing JA, Van Meter P, Woolnough DA (2010) Suspects and evidence: a review of the causes of extirpation and decline in freshwater mussels. Anim Biodivers Conserv 33(2):151–185

    Google Scholar 

  • Dubief B, Nunes FLD, Basuyaux O et al (2017) Immune priming and portal of entry effectors improve response to vibrio infection in a resistant population of the European abalone. Fish Shellfish Immunol 60:255–264

    CAS  PubMed  Google Scholar 

  • Duval D, Galinier R, Mouahid G et al (2015) A novel bacterial pathogen of Biomphalaria glabrata: a potential weapon for schistosomiasis control? PLoS Negl Trop Dis 9(2):e0003489

    PubMed  PubMed Central  Google Scholar 

  • Elston RA, Wilkinson MT (1985) Pathology, management and diagnosis of oyster velar virus-disease (OVVD). Aquaculture 48(3–4):189–210

    Google Scholar 

  • Epelboin Y, Quintric L, Guevelou E et al (2016) The kinome of Pacific oyster Crassostrea gigas, its expression during development and in response to environmental factors. PLoS One 11(5):e0155435

    PubMed  PubMed Central  Google Scholar 

  • Ertl NG, O’Connor WA, Papanicolaou A (2016) Transcriptome analysis of the Sydney rock oyster, Saccostrea glomerata: insights into molluscan immunity. PLoS One 11(6):e0156649

    PubMed  PubMed Central  Google Scholar 

  • Falfushynska H, Gnatyshyna L, Yurchak I et al (2016) Interpopulational variability of molecular responses to ionizing radiation in freshwater bivalves Anodontaanatina (Unionidae). Sci Total Environ 568:444–456

    CAS  PubMed  Google Scholar 

  • Farley CA, Banfield WG, Kasnic G Jr et al (1972) Oyster herpes-type virus. Science 178(4062):759–760

    CAS  PubMed  Google Scholar 

  • Fawcett LB, Tripp MR (1994) Chemotaxis of Mercenaria mercenaria hemocytes to bacteria in vitro. J Invertebr Pathol 63(3):275–284

    CAS  PubMed  Google Scholar 

  • Feng SY, Feng JS, Burke CN et al (1971) Light and electron microscopy of the leucocytes of Crassostrea virginica (Mollusca: Pelecypoda). Z Zellforsch Mikrosk Anat 120(2):222–245

    CAS  PubMed  Google Scholar 

  • Feng C, Ghosh A, Amin MN et al (2013) The galectin CvGal1 from the eastern oyster (Crassostrea virginica) binds to blood group A oligosaccharides on the hemocyte surface. J Biol Chem 288:24394–24409

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira-Rodriguez N, Pardo I (2017) The interactive effects of temperature, trophic status, and the presence of an exotic clam on the performance of a native freshwater mussel. Hydrobiologia 797(1):171–182

    CAS  Google Scholar 

  • Fisher MC, Henk DA, Briggs CJ et al (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484(7393):186–194

    CAS  PubMed  Google Scholar 

  • Fneich S, Theron A, Cosseau C et al (2016) Epigenetic origin of adaptive phenotypic variants in the human blood fluke Schistosoma mansoni. Epigenetics Chromatin 9:27

    PubMed  PubMed Central  Google Scholar 

  • Ford SE (1996) Range extension by the oyster parasite Perkinsus marinus into the northeastern United States: response to climate change? J Shellfish Res 15(1):45–56

    Google Scholar 

  • Ford SE, Stokes NA, Burreson EM et al (2009) Minchinia mercenariae n. sp (Haplosporidia) in the hard clam Mercenaria mercenaria: implications of a rare parasite in a commercially important host. J Eukaryot Microbiol 56(6):542–551

    CAS  PubMed  Google Scholar 

  • Foster JS, McFall-Ngai MJ (1998) Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Dev Genes Evol 208(6):295–303

    CAS  PubMed  Google Scholar 

  • Friedman CS, Andree KB, Beauchamp KA et al (2000) Candidatus Xenohaliotis californiensis, a newly described pathogen of abalone, Haliotis spp., along the west coast of North America. Int J Syst Evol Microbiol 50(Pt 2):847–855

    CAS  PubMed  Google Scholar 

  • Fryer SE, Adema CM (1993) Manipulation of Biomphalaria glabrata (Say) (Gastropoda, Planorbidae) hemocytes in vitro. J Moll Stud 59(Pt 4):371–379

    Google Scholar 

  • Fryer SE, Hull CJ, Bayne CJ (1989) Phagocytosis of yeast by Biomphalaria glabrata: carbohydrate specificity of hemocyte receptors and a plasma opsonin. Dev Comp Immunol 13(1):9–16

    CAS  PubMed  Google Scholar 

  • Fryer SE, Bender RC, Bayne CJ (1996) Inhibition of cysteine proteinase from Schistosoma mansoni larvae by alpha-macroglobulin from the plasma of Biomphalaria glabrata. J Parasitol 82(2):343–347

    CAS  PubMed  Google Scholar 

  • Gagnaire B, Frouin H, Moreau K et al (2006) Effects of temperature and salinity on haemocyte activities of the Pacific oyster, Crassostrea gigas (Thunberg). Fish Shellfish Immunol 20(4):536–547

    CAS  PubMed  Google Scholar 

  • Gagne F, Blaise C, Aoyama I et al. (2002) Biomarker study of a municipal effluent dispersion plume in two species of freshwater mussels. Environ Toxicol 17(3):149–159

    PubMed  Google Scholar 

  • Galinier R, Portela J, Mone Y et al (2013) Biomphalysin, a new beta pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathog 9(3):e1003216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galinier R, Tetreau G, Portet A et al (2017) First characterization of viruses from freshwater snails of the genus Biomphalaria, the intermediate host of the parasite Schistosoma mansoni. Acta Trop 167:196–203

    PubMed  Google Scholar 

  • Gantz VM, Jasinskiene N, Tatarenkova O et al (2015) Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc Natl Acad Sci U S A 112(49):e6736–e6743

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia C, Arzul I, Robert M et al (2009) Detection of atypical Marteilia refringens in mussels, Mytilus edulis in France. J Shellfish Res 28(3):688–688

    Google Scholar 

  • Gavery MR, Roberts SB (2014) A context dependent role for DNA methylation in bivalves. Brief Funct Genomics 13(3):217–222

    PubMed  Google Scholar 

  • Gerdol M (2017) Immune-related genes in gastropods and bivalves: a comparative overview. Invertebr Surviv J 14:103–118

    Google Scholar 

  • Gerdol M, Venier P (2015) An updated molecular basis for mussel immunity. Fish Shellfish Immunol 46(1):17–38

    CAS  PubMed  Google Scholar 

  • Gerdol M, Manfrin C, De Moro G et al (2011) The C1q domain containing proteins of the Mediterranean mussel Mytilus galloprovincialis: a widespread and diverse family of immune-related molecules. Dev Comp Immunol 35(6):635–643

    CAS  PubMed  Google Scholar 

  • Gestal C, Pallavicini A, Venier P et al (2010) MgC1q, a novel C1q-domain-containing protein involved in the immune response of Mytilus galloprovincialis. Dev Comp Immunol 34(9):926–934

    CAS  PubMed  Google Scholar 

  • Ghosh J, Buckley KM, Nair SV et al (2010) Sp185/333: a novel family of genes and proteins involved in the purple sea urchin immune response. Dev Comp Immunol 34(3):235–245

    CAS  PubMed  Google Scholar 

  • Giannelli A, Cantacessi C, ColeIla V et al (2016) Gastropod-borne helminths: a look at the snail–parasite interplay. Trends Parasitol 32(3):255–264

    PubMed  Google Scholar 

  • Gillis PL, Higgins SK, Jorge MB (2014) Evidence of oxidative stress in wild freshwater mussels (Lasmigona costata) exposed to urban-derived contaminants. Ecotoxicol Environ Saf 102:62–69

    CAS  PubMed  Google Scholar 

  • Gorbushin AM, Borisova EA (2015) Lectin-like molecules in transcriptome of Littorina littorea hemocytes. Dev Comp Immunol 48(1):210–220

    CAS  PubMed  Google Scholar 

  • Gorbushin AM, Iakovleva NV (2007) Functional characterization of Littorina littorea (Gastropoda: Prosobranchia) blood cells. J Mar Biol Assoc UK 87(3):741–746

    Google Scholar 

  • Gorbushin AM, Iakovleva NV (2011) A new gene family of single fibrinogen domain lectins in Mytilus. Fish Shellfish Immunol 30(1):434–438

    CAS  PubMed  Google Scholar 

  • Gordy MA, Pila EA, Hanington PC (2015) The role of fibrinogen-related proteins in the gastropod immune response. Fish Shellfish Immunol 46(1):39–49

    CAS  PubMed  Google Scholar 

  • Green TJ, Montagnani C (2013) Poly I:C induces a protective antiviral immune response in the Pacific oyster (Crassostrea gigas) against subsequent challenge with Ostreid herpesvirus (OsHV-1 mvar). Fish Shellfish Immunol 35:382–388

    CAS  PubMed  Google Scholar 

  • Green TJ, Robinson N, Chataway T et al (2014) Evidence that the major hemolymph protein of the Pacific oyster, Crassostrea gigas, has antiviral activity against herpesviruses. Antivir Res 110:168–174

    CAS  PubMed  Google Scholar 

  • Green TJ, Raftos D, Speck P et al (2015) Antiviral immunity in marine molluscs. J Gen Virol 96:2471–2482

    CAS  PubMed  Google Scholar 

  • Gromek SM, Suria AM, Fullmer MS et al (2016) Leisingera sp JC1, a bacterial isolate from Hawaiian bobtail squid eggs, produces indigoidine and differentially inhibits vibrios. Front Microbiol 7:1342

    PubMed  PubMed Central  Google Scholar 

  • Guo X, Ford SE (2016) Infectious diseases of marine molluscs and host responses as revealed by genomic tools. Philos Trans R Soc Lond Ser B Biol Sci 371(1689):20150206

    Google Scholar 

  • Guo X, He Y, Zhang L et al (2015) Immune and stress responses in oysters with insights on adaptation. Fish Shellfish Immunol 46(1):107–119

    CAS  PubMed  Google Scholar 

  • Hadden JW, Englard A, Sadlik JR et al (1979) The comparative effects of isoprinosine, levamisole, muramyl dipeptide and Sm1213 on lymphocyte and macrophage proliferation and activation in vitro. Int J Immunopharmacol 1(1):17–27

    CAS  PubMed  Google Scholar 

  • Hahn UK, Bender RC, Bayne CJ (2000) Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Dev Comp Immunol 24(6–7):531–541

    CAS  PubMed  Google Scholar 

  • Hahn UK, Bender RC, Bayne CJ (2001a) Killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata: role of reactive oxygen species. J Parasitol 87(2):292–299

    CAS  PubMed  Google Scholar 

  • Hahn UK, Bender RC, Bayne CJ (2001b) Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. J Parasitol 87(4):778–785

    CAS  PubMed  Google Scholar 

  • Hanington PC, Forys MA, Dragoo JW et al (2010) Role for a somatically diversified lectin in resistance of an invertebrate to parasite infection. Proc Natl Acad Sci U S A 107(49):21087–21092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hanington PC, Forys MA, Loker ES (2012) A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl Trop Dis 6(3):e1591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hanlon RT, Forsythe JW (1990) Diseases of Mollusca Cephalopoda diseases caused by microorganisms. In: Kinne O (ed) Diseases of marine animals, Vol. III. Introduction, Cephalopoda, Annelida, Crustacea, Chaetognatha, Echinodermata, Urochordata. Xv+696p. Biologische Anstalt Helgoland, Hamburg

    Google Scholar 

  • Hansen EL (1976) A cell line from embryos of Biomphalaria glabrata (Pulmonata): establishment and characteristics. In: Maramorosch K (ed) Invertebrate tissue culture, research applications. Academic Press, New York, pp 75–99

    Google Scholar 

  • Hasan I, Gerdol M, Fujii Y et al (2016) cDNA and gene structure of MytiLec-1, a bacteriostatic R-type lectin from the Mediterranean mussel (Mytilus galloprovincialis). Mar Drugs 14(5):92

    PubMed Central  Google Scholar 

  • Haseley SR, Vermeer HJ, Kamerling JP et al (2001) Carbohydrate self-recognition mediates marine sponge cellular adhesion. Proc Natl Acad Sci 98(16):9419–9424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haszprunar G, Wanninger A (2012) Molluscs. Curr Biol 22(13):R510–R514

    CAS  PubMed  Google Scholar 

  • Hata H, Kojima S (1989) Induction of resistance in Oncomelania hupensis nosophora against Schistosoma japonicum, but not against Paragonimus ohirai, using irradiated miracidia. Int J Parasitol 19(7):711–715

    CAS  PubMed  Google Scholar 

  • Hathaway JJM, Adema CM, Stout BA et al (2010) Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca). Dev Comp Immunol 34(4):425–435

    CAS  PubMed  Google Scholar 

  • He Y, Yu H, Haiyang B et al (2012) Mutation in promoter region of a serine protease inhibitor confers Perkinsus marinus resistance in the eastern oyster (Crassostrea virginica). Fish Shellfish Immunol 33(2):411–417

    CAS  PubMed  Google Scholar 

  • He Y, Jouaux A, Ford SE et al (2015) Transcriptome analysis reveals strong and complex antiviral response in a mollusc. Fish Shellfish Immunol 46(1):131–144

    CAS  PubMed  Google Scholar 

  • Hegaret H, Wikfors GH, Soudant P et al (2004) Immunological competence of eastern oysters, Crassostrea virginica, fed different microalgal diets and challenged with a temperature elevation. Aquaculture 234(1–4):541–560

    Google Scholar 

  • Hernroth B, Baden S, Tassidis H et al (2016) Impact of ocean acidification on antimicrobial activity in gills of the blue mussel (Mytilus edulis). Fish Shellfish Immunol 55:452–459

    CAS  PubMed  Google Scholar 

  • Hertel LA, Bayne CJ, Loker ES (2002) The symbiont Capsaspora owczarzaki, nov gen. nov sp., isolated from three strains of the pulmonate snail Biomphalaria glabrata is related to members of the Mesomycetozoea. Int J Parasitol 32(9):1183–1191

    CAS  PubMed  Google Scholar 

  • Hooper C, Day R, Slocombe R et al (2007) Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish Shellfish Immunol 22(4):363–379

    CAS  PubMed  Google Scholar 

  • Huang B, Zhang L, Tang X et al (2016) Genome-wide analysis of alternative splicing provides insights into stress adaptation of the Pacific oyster. Mar Biotechnol 18(5):598–609

    CAS  Google Scholar 

  • Huang B, Zhang L, Du Y et al (2017) Characterization of the mollusc RIG-I/MAVS pathway reveals an archaic antiviral signalling framework in invertebrates. Sci Rep 7:8217

    PubMed  PubMed Central  Google Scholar 

  • Humphries JE, Yoshino TP (2006) Schistosoma mansoni excretory–secretory products stimulate a p38 signalling pathway in Biomphalaria glabrata embryonic cells. Int J Parasitol 36(1):37–46

    CAS  PubMed  Google Scholar 

  • Hunter PJ, Runham NW (1970) Some aspects of recent research on slugs. Proc Malacol Soc London 39(2–3):235–238

    Google Scholar 

  • Ittiprasert W, Knight M (2012) Reversing the resistance phenotype of the Biomphalaria glabrata snail host Schistosoma mansoni infection by temperature modulation. PLoS Pathog 8(4):e1002677

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ittiprasert W, Nene R, Miller A, et al (2009) Schistosoma mansoni infection of juvenile Biomphalaria glabrata induces a differential stress response between resistant and susceptible snails. Exp Parasitol 123(3):203–211. https://doi.org/10.1016/j.exppara.2009.07.015.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ittiprasert W, Miller A, Knight M et al (2015) Evaluation of cytosine DNA methylation of the Biomphalaria glabrata heat shock protein 70 locus after biological and physiological stress. J Parasitol Vector Biol 7:182–193

    Google Scholar 

  • Ivanina AV, Hawkins C, Sokolova IM (2014) Immunomodulation by the interactive effects of cadmium and hypercapnia in marine bivalves Crassostrea virginica and Mercenaria mercenaria. Fish Shellfish Immunol 37(2):299–312

    CAS  PubMed  Google Scholar 

  • Ivanina AV, Hawkins C, Sokolova IM (2016) Interactive effects of copper exposure and environmental hypercapnia on immune functions of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Fish Shellfish Immunol 49:54–65

    CAS  PubMed  Google Scholar 

  • Iwanaga Y, Tsuji M (1985) Studies on host–parasite relationship between Schistosoma japonicum and Oncomelania snails 1. Antigenic communities between the Chinese strain of Schistosoma japonicum adult worm and Oncomelania snails. Jpn J Parasitol 34(1):1–6

    Google Scholar 

  • Jemaa M, Morin N, Cavelier P et al (2014) Adult somatic progenitor cells and hematopoiesis in oysters. J Exp Biol 217(17):3067–3077

    PubMed  Google Scholar 

  • Jeong KH, Lie KJ, Heyneman D (1980) Leucocytosis in Biomphalaria glabrata sensitized and resensitized to Echinostoma lindoense. J Invertebr Pathol 35(1):9–13

    CAS  PubMed  Google Scholar 

  • Jeong KH, Lie KJ, Heyneman D (1983) The ultrastructure of the amebocyte-producing organ in Biophalaria glabrata. Dev Comp Immunol 7(2):217–228

    CAS  PubMed  Google Scholar 

  • Jing X, Espinosa EP, Perrigault M et al (2011) Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica. Fish Shellfish Immunol 30(4–5):1207–1207

    Google Scholar 

  • Johnson MD (2011) The acquisition of phototrophy: adaptive strategies of hosting endosymbionts and organelles. Photosyn Res 107(1):117–132

    CAS  Google Scholar 

  • Kalinda C, Chimbari M, Mukaratirwa S (2017) Implications of changing temperatures on the growth, fecundity and survival of intermediate host snails of schistosomiasis: a systematic review. Int J Environ Res Public Health 14(1):80

    PubMed Central  Google Scholar 

  • Kang YS, Kim YM, Park KI et al (2006) Analysis of EST and lectin expressions in hemocytes of manila clams (Ruditapes philippinarum) (Bivalvia: Mollusca) infected with Perkinsus olseni. Dev Comp Immunol 30:1119–1131

    CAS  PubMed  Google Scholar 

  • Kocot KM, Cannon JT, Todt C et al (2011) Phylogenomics reveals deep molluscan relationships. Nature 477(7365):452–U101

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koropatnick TA, Kimbell JR, McFall-Ngai MJ (2007) Responses of host hemocytes during the initiation of the squid–Vibrio symbiosis. Biol Bull 212(1):29–39

    PubMed  Google Scholar 

  • Koropatnick T, Goodson MS, Heath-Heckman EAC et al (2014) Identifying the cellular mechanisms of symbiont-induced epithelial morphogenesis in the squid–Vibrio association. Biol Bull 226(1):56–68

    PubMed  PubMed Central  Google Scholar 

  • La Peyre JF, Chu FLE, Meyers JM (1995) Haemocytic and humoral activities of eastern and Pacific oysters following challenge by the protozoan Perkinsus marinus. Fish Shellfish Immunol 5:179–190

    Google Scholar 

  • La Peyre JF, Xue Q-G, Itoh N et al (2010) Serine protease inhibitor cvSI-1 potential role in the eastern oyster host defense against the protozoan parasite Perkinsus marinus. Dev Comp Immunol 34(1):84–92

    PubMed  Google Scholar 

  • Larson MK, Bender RC, Bayne CJ (2014) Resistance of Biomphalaria glabrata 13–16-R1 snails to Schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes. Int J Parasitol 44:343–353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Le Clec’h W, Anderson TJC, Chevalier FD (2016) Characterization of hemolymph phenoloxidase activity in two Biomphalaria snail species and impact of Schistosoma mansoni infection. Parasit Vectors 9:32

    PubMed  PubMed Central  Google Scholar 

  • Lefcort H, Bayne CJ (1991) Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni (Trematoda). Parasitology 103(Pt 3):357–362

    PubMed  Google Scholar 

  • Leicht K, Seppälä O (2014) Infection success of Echinoparyphium aconiatum (Trematoda) in its snail host under high temperature: role of host resistance. Parasit Vectors 7:192

    PubMed  PubMed Central  Google Scholar 

  • Leicht K, Jokela J, Seppälä O (2013) An experimental heat wave changes immune defense and life history traits in a freshwater snail. Ecol Evol 3:4861–4871

    PubMed  PubMed Central  Google Scholar 

  • Leite RB, Milan M, Coppe A et al (2013) mRNA-Seq and microarray development for the grooved carpet shell clam, Ruditapes decussatus: a functional approach to unravel host–parasite interaction. BMC Genomics 14:741

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis SL, Maslin MA (2015) Geological evidence for the Anthropocene. Science 349(6245):246–247

    CAS  PubMed  Google Scholar 

  • Li Y, Song X, Wang W et al (2017) The hematopoiesis in gill and its role in the immune response of Pacific oyster Crassostrea gigas against secondary challenge with Vibrio splendidus. Dev Comp Immunol 71:59–69

    CAS  PubMed  Google Scholar 

  • Lie KJ (1982) Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata: a discussion of the interference theory. Trop Geogr Med 34(2):111–122

    CAS  PubMed  Google Scholar 

  • Lie KJ, Heyneman D (1976) Studies on resistance in snails. 3. Tissue reactions to Echinostoma lindoense sporocysts in sensitized and resensitized Biomphalaria glabrata. J Parasitol 62(1):51–58

    CAS  PubMed  Google Scholar 

  • Lie KJ, Heyneman D, Yau P (1975) Origin of amebocytes in Biomphalaria glabrata. J Parasitol 61(3):574–576

    Google Scholar 

  • Lie KJ, Jeong KH, Heyneman D (1982) Further characterization of acquired-resistance in Biomphalaria glabrata. J Parasitol 68(4):529–531

    CAS  PubMed  Google Scholar 

  • Lie KJ, Jeong KH, Heyneman D (1983) Acquired resistance in snails: induction of resistance to Schistosoma mansoni in Biomphalaria glabrata. Int J Parasitol 13(3):301–304

    CAS  PubMed  Google Scholar 

  • Liscovitch-Brauer N, Alon S, Porath HT et al (2017) Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169(2):191–202

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lockyer AE, Noble LR, Rollinson D et al (2004) Schistosoma mansoni: resistant specific infection-induced gene expression in Biomphalaria glabrata identified by fluorescent-based differential display. Exp Parasitol 107(1–2):97–104

    CAS  PubMed  Google Scholar 

  • Lockyer AE, Spinks J, Kane RA et al (2008) Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 9:634. https://doi.org/10.1186/1471-2164-9-634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lodes MJ, Yoshino TP (1990) The effect of schistosome excretory secretory products on Biomphalaria glabrata hemocyte motility. J Invertebr Pathol 56(1):75–85

    CAS  PubMed  Google Scholar 

  • Lohan KMP, Hill-Spanik KM, Torchin ME et al (2016) Richness and distribution of tropical oyster parasites in two oceans. Parasitology 143(9):1119–1132

    Google Scholar 

  • Loker ES (2010) Gastropod immunobiology. In: Soderhall K (ed) Invertebrate immunity. Advances in experimental medicine and biology, vol 708. Springer, New York, pp 17–43

    Google Scholar 

  • Loker ES, Bayne CJ (2001) Molecular studies of the molluscan response to digenean infection. In: Beck G, Sugumaran M, Cooper E (eds) Phylogenetic perspectives on the vertebrate immune system. Kluwer Academic/Plenum, New York, pp 209–222

    Google Scholar 

  • Loker ES, Hertel LA (1987) Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. J Parasitol 73(3):503–513

    CAS  PubMed  Google Scholar 

  • Loker ES, Bayne CJ, Buckley PM (1982) Ultrastructure of encapsulation of Schistosoma mansoni mother sporocysts by hemocytes of juveniles of the 10-r2 strain of Biomphalaria glabrata. J Parasitol 68(1):84–94

    CAS  PubMed  Google Scholar 

  • Loker ES, Cimino DF, Hertel LA (1992) Excretory–secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria flabrata hemocyte functions. J Parasitol 78(1):104–115

    CAS  PubMed  Google Scholar 

  • Loker ES, Couch L, Hertel LA (1994) Elevated agglutination titers in plasma of Biomphalaria glabrata exposed to Echinostoma paraensei: characterization and functional relevance of a trematode-induced response. Parasitology 108(Pt 1):7–26

    Google Scholar 

  • Lydeard C, Cowie RH, Ponder WF et al (2004) The global decline of nonmarine mollusks. Bioscience 54(4):321–330

    Google Scholar 

  • Mahapatra E, Dasgupta D, Bhattacharya N et al (2017) Sustaining immunity during starvation in bivalve mollusc: a costly affair. Tissue Cell 49(2, Pt B):239–248

    PubMed  Google Scholar 

  • Malham SK, Runham NW, Secombes CJ (1998) Lysozyme and antiprotease activity in the lesser octopus Eledone cirrhosa (Lam.) (Cephalopoda). Dev Comp Immunol 22(1):27–37

    CAS  PubMed  Google Scholar 

  • Mangal TD, Paterson S, Fenton A (2008) Predicting the impact of long-term temperature changes on the epidemiology and control of schistosomiasis: a mechanistic model. PLoS One 3(1):e1438

    PubMed  PubMed Central  Google Scholar 

  • Martins-Souza RL, Pereira CAJ, Coelho PMZ et al (2009) Flow cytometry analysis of the circulating haemocytes from Biomphalaria glabrata and Biomphalaria tenagophila following Schistosoma mansoni infection. Parasitology 136(1):67–76

    CAS  PubMed  Google Scholar 

  • Mas-Coma S, Adela Valero M, Dolores Bargues M (2009) Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol 163(4):264–280

    PubMed  Google Scholar 

  • Matozzo V, Marin MG (2011) Bivalve immune responses and climate changes: is there a relationship? Invertebr Surviv J 8(1):70–77

    Google Scholar 

  • McAnulty SJ, Nyholm SV (2017) The role of hemocytes in the Hawaiian bobtail squid, Euprymna scolopes: a model organism for studying beneficial host–microbe interactions. Front Microbiol 7:2013

    PubMed  PubMed Central  Google Scholar 

  • McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10(5):190–194

    CAS  PubMed  Google Scholar 

  • McCreesh N, Booth M (2013) Challenges in predicting the effects of climate change on Schistosoma mansoni and Schistosoma haematobium transmission potential. Trends Parasitol 29(11):548–555

    PubMed  Google Scholar 

  • McCreesh N, Nikulin G, Booth M (2015) Predicting the effects of climate change on Schistosoma mansoni transmission in eastern Africa. Parasit Vectors 8:4

    PubMed  PubMed Central  Google Scholar 

  • McDowell IC, Modak TH, Lane CE et al (2016) Multi-species protein similarity clustering reveals novel expanded immune gene families in the eastern oyster Crassostrea virginica. Fish Shellfish Immunol 53:13–23

    CAS  PubMed  Google Scholar 

  • McFall-Ngai MJ (2014) Divining the essence of symbiosis: insights from the squid–Vibrio model. PLoS Biol 12(2):e1001783

    PubMed  PubMed Central  Google Scholar 

  • McLean N (1980) Phagocytosis by epidermal-cells of the mantle in Mytilus edulis L. (Mollusca, Bivalvia). Comp Biochem Physiol 66(2):367–369

    Google Scholar 

  • Metzger MJ, Reinisch C, Sherry J et al (2015) Horizontal transmission of clonal cancer cells causes leukemia in soft-shell clams. Cell 161(2):255–263

    CAS  PubMed  PubMed Central  Google Scholar 

  • Metzger MJ, Villalba A, Carballal MJ et al (2016) Widespread transmission of independent cancer lineages within multiple bivalve species. Nature 534(7609):705–709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyers TR, Burton T, Evans W, Starkey N (2009) Detection of viruses and virus-like particles in four species of wild and farmed bivalve molluscs in Alaska, USA, from 1987 to 2009. Dis Aquat Org 88:1–12

    Google Scholar 

  • Michelson EH, Dubois L (1977) Agglutinins and lysins in molluscan family Planorbidae: survey of hemolymph, egg-masses, and albumen-gland extracts. Biol Bull 153(1):219–227

    CAS  PubMed  Google Scholar 

  • Miller RL, Collawn JF, Fish WW (1982) Purification and macromolecular properties of a sialic acid-specific lectin from the slug Limax flavus. J Biol Chem 257(13):7574–7580

    CAS  PubMed  Google Scholar 

  • Milutinovic B, Kurtz J (2016) Immune memory in invertebrates. Semin Immunol 28(4):328–342

    CAS  PubMed  Google Scholar 

  • Mitta G, Vandenbulcke F, Roch P (2000) Original involvement of antimicrobial peptides in mussel innate immunity. FEBS Lett 486(3):185–190

    CAS  PubMed  Google Scholar 

  • Mitta G, Gourbal B, Grunau C et al (2017) The compatibility between Biomphalaria glabrata snails and Schistosoma mansoni: an increasingly complex puzzle. Adv Parasitol 97:111–145

    CAS  PubMed  Google Scholar 

  • Mone Y, Gourbal B, Duval D et al (2010) A large repertoire of parasite epitopes matched by a large repertoire of host immune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis 4(9):e813

    PubMed  PubMed Central  Google Scholar 

  • Murchison EP (2016) Cancer: transmissible tumours under the sea. Nature 534(7609):628–629

    CAS  PubMed  Google Scholar 

  • Nelson MK, Cruz BC, Buena KL et al (2016) Effects of abnormal temperature and starvation on the internal defense system of the schistosome-transmitting snail Biomphalaria glabrata. J Invertebr Pathol 138:18–23

    PubMed  PubMed Central  Google Scholar 

  • Newton K, Peters R, Raftos D (2004) Phenoloxidase and QX disease resistance in Sydney rock oysters (Saccostrea glomerata). Dev Comp Immunol 28(6):565–569

    CAS  PubMed  Google Scholar 

  • Nicolai A, Ansart A (2017) Conservation at a slow pace: terrestrial gastropods facing fast-changing climate. Conserv Physiol 5:1–17

    Google Scholar 

  • Nikapitiya C, Kim W-S, Park K et al (2014) Identification of potential markers and sensitive tissues for low or high salinity stress in an intertidal mud crab (Macrophthalmus japonicus). Fish Shellfish Immunol 41(2):407–416

    CAS  PubMed  Google Scholar 

  • Nyholm SV, McFall-Ngai MJ (2004) The winnowing: establishing the squid–Vibrio symbiosis. Nat Rev Microbiol 2(8):632–642

    CAS  PubMed  Google Scholar 

  • Nyholm SV, Stewart JJ, Ruby EG et al (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11(2):483–493

    PubMed  PubMed Central  Google Scholar 

  • Olafsen JA, Fletcher TC, Grant PT (1992) Agglutinin activity in Pacific oyster (Crassostrea gigas) emolymph following in vivo Vibrio anguillarum challenge. Dev Comp Immunol 16:123–138

    CAS  PubMed  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV et al (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    CAS  PubMed  Google Scholar 

  • Ottaviani E, Accorsi A, Rigillo G et al (2013) Epigenetic modification in neurons of the mollusc Pomacea canaliculata after immune challenge. Brain Res 1537:18–26

    CAS  PubMed  Google Scholar 

  • Owczarzak A, Stibbs HH, Bayne CJ (1980) The destruction of Schistosoma mansoni mother sporocysts in vitro by amebas isolated from Biomphalaria glabrata: an ultrastructural study. J Invertebr Pathol 35(1):26–33

    CAS  PubMed  Google Scholar 

  • Papalexi E, Satija R (2017) Single-cell RNA sequencing to explore immune cell heterogeneity. Nat Rev Immunol. https://doi.org/10.1038/nri.2017.76

    PubMed  Google Scholar 

  • Paull SH, Johnson PTJ (2011) High temperature enhances host pathology in a snail–trematode system: possible consequences of climate change for the emergence of disease. Freshw Biol 56(4):767–778

    Google Scholar 

  • Paynter AN, Metzger MJ, Sessa JA et al (2017) Evidence of horizontal transmission of the cancer-associated Steamer retrotransposon among ecological cohort bivalve species. Dis Aquat Org 124(2):165–168

    Google Scholar 

  • Perrigault M, Bugge DM, Allam B (2010) Effect of environmental factors on survival and growth of quahog parasite unknown (QPX) in vitro. J Invertebr Pathol 104(2):83–89

    PubMed  Google Scholar 

  • Perrigault M, Dahl SF, EPales E et al (2011) Effects of temperature on hard clam (Mercenaria mercenaria) immunity and QPX (Quahog Parasite Unknown) disease development: II. Defense parameters. J Invertebr Pathol 106(2):322–332

    PubMed  Google Scholar 

  • Perry KJ, Henry JQ (2015) CRISPR/Cas9-mediated genome modification in the mollusc, Crepidula fornicate. Genesis 53(2):237–244

    CAS  PubMed  Google Scholar 

  • Pila EA, Sullivan JT, Wu XZ et al (2016a) Haematopoiesis in molluscs: a review of haemocyte development and function in gastropods, cephalopods and bivalves. Dev Comp Immunol 58:119–128

    CAS  PubMed  Google Scholar 

  • Pila EA, Gordy MA, Phillips VK et al (2016b) Endogenous growth factor stimulation of hemocyte proliferation induces resistance to Schistosoma mansoni challenge in the snail host. Proc Natl Acad Sci U S A 113(19):5305–5310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pila EA, Tarrabain M, Kabore AL et al (2016c) A novel toll-like receptor (TLR) influences compatibility between the gastropod Biomphalaria glabrata and the digenean trematode Schistosoma mansoni. PLoS One 11(3):e1005513

    Google Scholar 

  • Pila EA, Li H, Hambrook JR et al (2017) Schistosomiasis from a snail’s perspective: advances in snail immunity. Trends Parasitol 33(11):845–857. https://doi.org/10.1016/j.pt.2017.07.006

    Article  PubMed  Google Scholar 

  • Pinaud S, Portela J, Duval D et al (2016) A shift from cellular to humoral responses contributes to innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathog 12(1):e1005361

    PubMed  PubMed Central  Google Scholar 

  • Plows LD, Cook RT, Davies AJ et al (2006) Phagocytosis by Lymnaea stagnalis haemocytes: a potential role for phosphatidylinositol 3-kinase but not protein kinase A. J Invertebr Pathol 91(1):74–77

    CAS  PubMed  Google Scholar 

  • Ponder WF, Lindberg DR (eds) (2008) Phylogeny and evolution of the Mollusca. University of California Press, Berkeley

    Google Scholar 

  • Port F, Chen H-M, Lee T et al (2014) Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc Natl Acad Sci U S A 111(29):e2967–e2976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Portela J, Duval D, Rognon A et al (2013) Evidence for specific genotype-dependent immune priming in the lophotrochozoan Biomphalaria glabrata snail. J Innate Immun 5(3):261–276

    CAS  PubMed  PubMed Central  Google Scholar 

  • Portet A, Pinaud S, Tetreau G et al (2017) Integrated multi-omic analyses in Biomphalaria–Schistosoma dialogue reveal the immunobiological significance of FREP-SmPoMuc interaction. Dev Comp Immunol 75:16–27

    CAS  PubMed  Google Scholar 

  • Prado-Alvarez M, Rotllant J, Gestal C et al (2009) Characterization of a C3 and a factor B–like in the carpet-shell clam, Ruditapes decussatus. Fish Shellfish Immunol 26(2):305–315

    CAS  PubMed  Google Scholar 

  • Queiroz FR, Silva LM, Jeremias WJ et al (2017) Differential expression of small RNA pathway genes associated with the Biomphalaria glabrata/Schistosoma mansoni interaction. PLoS One 12(7):e0181483

    PubMed  PubMed Central  Google Scholar 

  • Raftos DA, Kuchel R, Aladaileh S et al (2014) Infectious microbial diseases and host defense responses in Sydney rock oysters. Front Microbiol 5:135

    PubMed  PubMed Central  Google Scholar 

  • Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38(2):127–145

    Google Scholar 

  • Ramilo A, Pintado J, Villalba A et al (2016) Perkinsus olseni and P. chesapeaki detected in a survey of perkinsosis of various clam species in Galicia (NW Spain) using PCR-DGGE as a screening tool. J Invertebr Pathol 133:50–58

    CAS  PubMed  Google Scholar 

  • Ren W, Chen H, Renault T et al (2013) Complete genome sequence of acute viral necrosis virus associated with massive mortality outbreaks in the Chinese scallop, Chlamys farreri. Virol J 10:110

    CAS  PubMed  PubMed Central  Google Scholar 

  • Renwrantz L (1983) Involvement of agglutinins (lectins) in invertebrate defense reactions: the immuno-biological importance of carbohydrate-specific binding-molecules. Dev Comp Immunol 7(4):603–608

    CAS  Google Scholar 

  • Renwrantz LR, Richards EH (1992) Recognition of beta-glucuronidase by the calcium-independent phosphomannosyl surface receptor of haemocytes from the gastropod mollusc, Helix pomatia. Dev Comp Immunol 16(2–3):251–256

    CAS  PubMed  Google Scholar 

  • Renwrantz L, Spielvogel F (2011) Heart rate and hemocyte number as stress indicators in disturbed hibernating vineyard snails, Helix pomatia. Comp Biochem Physiol A Mol Integr Physiol 160(4):467–473. https://doi.org/10.1016/j.cbpa.2011.08.002

    Article  CAS  PubMed  Google Scholar 

  • Renwrantz L, Stahmer A (1983) Opsonizing properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis. J Comp Physiol 149:535–546

    CAS  Google Scholar 

  • Richards GP, Watson MA, Needleman DS et al (2015) Mortalities of eastern and Pacific oyster larvae caused by the pathogens Vibrio coralliilyticus and Vibrio tubiashii. Appl Environ Microbiol 81(1):292–297

    PubMed  Google Scholar 

  • Ridgway I, Bowden TJ, Roman-Gonzalez A et al (2014) Resistance to oxidative stress is not associated with the exceptional longevity of the freshwater pearl mussel, Margaritifera margaritifera nor three unionid species. Aquat Sci 76(2):259–267

    CAS  Google Scholar 

  • Rinkevich B (2011) Cell cultures from marine invertebrates: new insights for capturing endless stemness. Mar Biotechnol 13(3):345–354

    CAS  Google Scholar 

  • Rodríguez de la Vega RC, Possani LD (2005) On the evolution of invertebrate defensins. Trends Genet 21:330–332

    PubMed  Google Scholar 

  • Romero A, Dios S, Poisa-Beiro L et al (2011) Individual sequence variability and functional activities of fibrinogen-related proteins (FREPs) in the Mediterranean mussel (Mytilus galloprovincialis) suggest ancient and complex immune recognition models in invertebrates. Dev Comp Immunol 35(3):334–344

    CAS  PubMed  Google Scholar 

  • Rosani U, Pallavicini A, Venice P (2016) The miRNA biogenesis in marine bivalves. PeerJ 4:e1763

    PubMed  PubMed Central  Google Scholar 

  • Rungger D, Rastelli M, Braendle E et al (1971) Virus-like particle associated with lesions in muscles of Octopus vulgaris. J Invertebr Pathol 17(1):72–80

    Google Scholar 

  • Salazar KA, Joffe NR, Dinguirard N et al (2015) Transcriptome analysis of the white body of the squid Euprymna tasmanica with emphasis on immune and hematopoietic gene discovery. PLoS One 10(3):e0119949

    PubMed  PubMed Central  Google Scholar 

  • Salice CJ, Roesijadi G (2002) Resistance to cadmium and parasite infection are inversely related in two strains of a freshwater gastropod. Environ Toxicol Chem 21(7):1398–1403

    CAS  PubMed  Google Scholar 

  • Salice CJ, Anderson TA, Roesijadi G (2010) Adaptive responses and latent costs of multigeneration cadmium exposure in parasite resistant and susceptible strains of a freshwater snail. Ecotoxicology 19(8):1466–1475

    CAS  PubMed  Google Scholar 

  • Sauve S, Brousseau P, Pellerin J et al (2002) Phagocytic activity of marine and freshwater bivalves: in vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquat Toxicol 58(3–4):189–200

    CAS  PubMed  Google Scholar 

  • Savin KW, Cocks BG, Wong F et al (2010) A neurotropic herpesvirus infecting the gastropod, abalone, shares ancestry with oyster herpesvirus and a herpesvirus associated with the amphioxus genome. Virol J 7:308

    PubMed  PubMed Central  Google Scholar 

  • Schmitt P, Gueguen Y, Desmarais E et al (2010) Molecular diversity of antimicrobial effectors in the oyster Crassostrea gigas. BMC Evol Biol 10:23

    PubMed  PubMed Central  Google Scholar 

  • Schneeweiss H, Renwrantz L (1993) Analysis of the attraction of hemocytes from Mytilus edulis by molecules of bacterial origin. Dev Comp Immunol 17(5):377–387

    CAS  PubMed  Google Scholar 

  • Schultz JH, Adema CM (2017) Comparative immunogenomics of molluscs. Dev Comp Immunol 75:3–15

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartzman JA, Koch E, Heath-Heckman EAC et al (2015) The chemistry of negotiation: rhythmic, glycan-driven acidification in a symbiotic conversation. Proc Natl Acad Sci U S A 112(2):566–571

    CAS  PubMed  Google Scholar 

  • Segarra A, Mauduit F, Faury N et al (2014) Dual transcriptomics of virus–host interactions: comparing two Pacific oyster families presenting contrasted susceptibility to ostreid herpesvirus 1. BMC Genomics 15:580–592

    PubMed  PubMed Central  Google Scholar 

  • Seo J-K, Lee MJ, Nam B-H et al (2013) cgMolluscidin, a novel dibasic residue repeat rich antimicrobial peptide, purified from the gill of the Pacific oyster, Crassostrea gigas. Fish Shellfish Immunol 35(2):480–488

    CAS  PubMed  Google Scholar 

  • Seppälä O, Jokela J (2011) Immune defence under extreme ambient temperature. Biol Lett 7:119–122

    PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    CAS  PubMed  Google Scholar 

  • Sire C, Rognon A, Theron A (1998) Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism? Parasitology 117(Pt 2):117–122

    PubMed  Google Scholar 

  • Sohn E (2017) Hothouse of disease. Nature 543(7647):S44–S46

    CAS  PubMed  Google Scholar 

  • Soldánová M, Kuris AM, Scholz T et al (2012) The role of spatial and temporal heterogeneity and competition in structuring trematode communities in the great pond snail, Lymnaea stagnalis (L.). J Parasitol 98(3):460–471

    PubMed  Google Scholar 

  • Song X, Zhang H, Zhao J et al (2010) An immune responsive multidomain galectin from bay scallop Argopectens irradians. Fish Shellfish Immunol 28:326–332

    CAS  PubMed  Google Scholar 

  • Song X, Wang H, Xin L et al (2016) The immunological capacity in the larvae of Pacific oyster Crassostrea gigas. Fish Shellfish Immunol 49:461–469

    CAS  PubMed  Google Scholar 

  • Sullivan JT, Farengo DA (2002) Survival of heterotopic heart xenografts from Helisoma duryi, Planorbula armigera, and Planorbarius corneus in Biomphalaria glabrata (Pulmonata, Basommatophora, Planorbidae): evidence for phylogenetic relatedness? Invertebr Biol 121(1):38–46

    Google Scholar 

  • Sullivan JT, Spence JV (1994) Transfer of resistance to Schistosoma mansoni in Biomphalaria glabrata by allografts of amebocyte-producing organ. J Parasitol 80:449–453

    CAS  PubMed  Google Scholar 

  • Sullivan JT, Weir GO, Brammer SR (1993) Heterotopic heart-transplants in Biomphalaria glabrata (Mollusca, Pulmonata): fate of congeneric xenografts. Dev Comp Immunol 17(6):467–474

    CAS  PubMed  Google Scholar 

  • Sullivan JT, Brammer SR, Hargraves CD et al (1995a) Heterotopic heart-transplants in Biomphalaria glabrata (Mollusca, Pulmonata): fate of xenografts from 7 pulmonate genera. Invertebr Biol 114(2):151–160

    Google Scholar 

  • Sullivan JT, Spence JV, Nunez JK (1995b) Killing of Schistosoma mansoni sporocysts in Biomphalaria glabrata implanted with amebocyte-producing organ allografts from resistant snails. J Parasitol 81(5):829–833

    CAS  PubMed  Google Scholar 

  • Sullivan JT, Galvan AG, Lares RR (1999) Survival of heterotopic headfoot transplants in Biomphalaria glabrata (Mollusca: Pulmonata). Invertebr Biol 118(1):63–67

    Google Scholar 

  • Sun Y, Zhang L, Zhang M et al (2016) Characterization of three mitogen-activated protein kinases (MAPK) genes reveals involvement of ERK and JNK, not p38 in defense against bacterial infection in Yesso scallop Patinopecten yessoensis. Fish Shellfish Immunol 54:507–515

    CAS  PubMed  Google Scholar 

  • Syed NI, Ridgway RL, Lukowiak K et al (1992) Transplantation and functional-integration of an identified respiratory interneuron in Lymnaea stagnalis. Neuron 8(4):767–774

    CAS  PubMed  Google Scholar 

  • Tanguy A, Guo XM, Ford SE (2004) Discovery of genes expressed in response to Perkinsus marinus challenge in Eastern (Crassostrea virginica) and Pacific (C. gigas) oysters. Gene 338(1):121–131

    CAS  PubMed  Google Scholar 

  • Tasumi S, Vasta GR (2007) A galectin of unique domain organization from hemocytes of the eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J Immunol 179(5):3086–3098

    CAS  PubMed  Google Scholar 

  • Tennessen JA, Bonner KM, Bollmann SR et al (2015a) Genome-wide scan and test of candidate genes in the snail Biomphalaria glabrata reveal new locus influencing resistance to Schistosoma mansoni. PLoS Negl Trop Dis 9(9):e0004077

    PubMed  PubMed Central  Google Scholar 

  • Tennessen JA, Theron A, Marine M et al (2015b) Hyperdiverse gene cluster in snail host conveys resistance to human Schistosome parasites. PLoS Genet 11(3):e1005067

    PubMed  PubMed Central  Google Scholar 

  • Tirape A, Bacque C, Brizard R et al (2007) Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev Comp Immunol 31(9):859–873

    CAS  PubMed  Google Scholar 

  • Travers M-A, Basuyaux O, Le Goic N et al (2009) Influence of temperature and spawning effort on Haliotis tuberculata mortalities caused by Vibrio harveyi: an example of emerging vibriosis linked to global warming. Glob Chang Biol 15(6):1365–1376

    Google Scholar 

  • Tripp MR (1974) Molluscan immunity. Ann N Y Acad Sci 234:23–27

    CAS  PubMed  Google Scholar 

  • Vasta GR, Sullivan JT, Cheng TC et al (1982) A cell membrane–associated lectin of the oyster hemocyte. J Invertebr Pathol 40(3):367–377

    CAS  Google Scholar 

  • Vasta GR, Cheng TC, Marchalonis JJ (1984) A lectin on the hemocyte membrane of the oyster (Crassostrea virginica). Cell Immunol 88(2):475–488

    CAS  PubMed  Google Scholar 

  • Vasta GR, Ahmed H, Tasumi S et al (2007) Biological roles of lectins in innate immunity: molecular and structural basis for diversity in self/non-self recognition. In: Current topics in innate immunity. Springer-Verlag, Berlin, pp 389–406

    Google Scholar 

  • Vasta GR, Feng C, Bianchet MA et al (2015) Structural, functional, and evolutionary aspects of galectins in aquatic mollusks: from a sweet tooth to the Trojan horse. Fish Shellfish Immunol 46(1):94–106

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vea IM, Siddall ME (2011) Scanning electron microscopy and molecular characterization of a new haplosporidium species (Haplosporidia), a parasite of the marine gastropod Siphonaria pectinata (Mollusca: Gastropoda: Siphonariidae) in the Gulf of Mexico. J Parasitol 97(6):1062–1066

    PubMed  Google Scholar 

  • Vergote D, Bouchut A, Sautiere PE et al (2005) Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 35(2):215–224

    CAS  PubMed  Google Scholar 

  • Walker AJ, Lacchini AH, Sealey KL et al (2010) Spreading by snail (Lymnaea stagnalis) defence cells is regulated through integrated PKC, FAK and Src signaling. Cell Tissue Res 341(1):131–145

    CAS  PubMed  Google Scholar 

  • Wang F, Meng Q, Tang X et al (2013) The long-term variability of sea surface temperature in the seas east of China in the past 40 a. Acta Oceanol Sin 32:48–53

    CAS  Google Scholar 

  • Wang L, Yue F, Song X et al (2015) Maternal immune transfer in mollusc. Dev Comp Immunol 48(2):354–359

    CAS  PubMed  Google Scholar 

  • Wang K, Espinosa EP, Allam B (2016) Effect of “heat shock” treatments on QPX disease and stress response in the hard clam, Mercenaria mercenaria. J Invertebr Pathol 138:39–49

    PubMed  Google Scholar 

  • Wang W, Li M, Wang L et al (2017a) The granulocytes are the main immunocompetent hemocytes in Crassostrea gigas. Dev Comp Immunol 67:221–228

    CAS  PubMed  Google Scholar 

  • Wang L, Song X, Song L (2017b) The oyster immunity. Dev Comp Immunol. https://doi.org/10.1016/j.dci.2017.05.025

    CAS  Google Scholar 

  • Waters CN, Zalasiewicz J, Summerhayes C et al (2016) The Anthropocene is functionally and stratigraphically distinct from the Holocene. Science 351(6269):aad2622

    PubMed  Google Scholar 

  • Weiss BL, Maltz M, Aksoy S (2012) Obligate symbionts activate immune system development in the tsetse fly. J Immunol 188(7):3395–3403

    CAS  PubMed  Google Scholar 

  • Wendling CC, Wegner KM (2013) Relative contribution of reproductive investment, thermal stress and Vibrio infection to summer mortality phenomena in Pacific oysters. Aquaculture 412:88–96

    Google Scholar 

  • Wu X-J, Dinguirard N, Sabat G et al (2017) Proteomic analysis of Biomphalaria glabrata plasma proteins with binding affinity to those expressed by early developing larval Schistosoma mansoni. PLoS Pathog 13(5):e1006081. https://doi.org/10.1371/journal.ppat.1006081

    PubMed  PubMed Central  Google Scholar 

  • Xing J, Espinosa EP, Perrigault M, Allam B (2011) Identification, molecular characterization and expression analysis of a mucosal C-type lectin in the eastern oyster, Crassostrea virginica. Fish Shellfish Immunol 30:851–858

    Google Scholar 

  • Xu G, Greene GH, Yoo H et al (2017) Global translational reprogramming is a fundamental layer of immune regulation in plants. Nature 545(7655):487–490

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang C, Wang L, Zhang H et al (2014) A new fibrinogen-related protein from Argopecten irradians (AiFREP-2) with broad recognition spectrum and bacteria agglutination activity. Fish Shellfish Immunol 38:221–229

    CAS  PubMed  Google Scholar 

  • Yonge CM (1926) Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J Mar Biol Assoc UK 14(2):295–386

    Google Scholar 

  • Yoshino TP, Bayne CJ (1983) Mimicry of snail host antigens by miracidia and primary sporocysts of Schistosoma mansoni. Parasite Immunol 5(3):317–328

    CAS  PubMed  Google Scholar 

  • Yoshino TP, Dinguirard N, Kunert J et al (2008) Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411(1–2):46–58

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshino TP, Bickham U, Bayne CJ (2013a) Molluscan cells in culture: primary cell cultures and cell lines. Can J Zool 91(6):391–404

    Google Scholar 

  • Yoshino TP, Wu X-J, Gonzalez LA et al (2013b) Circulating Biomphalaria glabrata hemocyte subpopulations possess shared schistosome glycans and receptors capable of binding larval glycoconjugates. Exp Parasitol 133(1):28–36

    CAS  PubMed  Google Scholar 

  • Yu Y, Yang X, Wang H et al (2013) Cytosine methylation alteration in natural populations of Leymus chinensis induced by multiple abiotic stresses. PLoS One 8(2):e55772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yue F, Shi X, Zhou Z et al (2013) The expression of immune-related genes during the ontogenesis of scallop Chlamys farreri and their response to bacterial challenge. Fish Shellfish Immunol 34(3):855–864

    CAS  PubMed  Google Scholar 

  • Zahoor Z, Davies AJ, Kirk RS et al (2009) Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal–regulated kinase pathway. Parasit Vectors 2(18):1–10

    Google Scholar 

  • Zanjani NT, Sairi F, Marshall G et al (2014) Formulation of abalone hemocyanin with high antiviral activity and stability. Eur J Pharm Sci 53:77–85

    CAS  PubMed  Google Scholar 

  • Żbikowska E, Żbikowski J (2015) Digenean larvae—the cause and beneficiaries of the changes in host snails’ thermal behavior. Parasitol Res 114(3):1063–1070

    PubMed  PubMed Central  Google Scholar 

  • Zelck UE, Gege BE, Schmid S (2007) Specific inhibitors of mitogen-activated protein kinase and P13-K pathways impair immune responses by hemocytes of trematode intermediate host snails. Dev Comp Immunol 31(4):321–331

    CAS  PubMed  Google Scholar 

  • Zhang S-M, Adema CM, Kepler TB et al (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305(5681):251–254

    CAS  PubMed  Google Scholar 

  • Zhang D, Ma J, Jiang J et al (2010) Molecular characterization and expression analysis of lipopolysaccharide and beta-1,3-glucan-binding protein (LGBP) from pearl oyster Pinctada fucata. Mol Biol Rep 37(7):3335–3343

    CAS  PubMed  Google Scholar 

  • Zhang G, Fang X, Guo X et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490(7418):49–54

    CAS  PubMed  Google Scholar 

  • Zhang T, Qiu L, Sun Z et al (2014) The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol 45(1):141–150

    CAS  PubMed  Google Scholar 

  • Zhang S-M, Buddenborg SK, Adema CM et al (2015a) Altered gene expression in the Schistosome-transmitting snail Biomphalaria glabrata following exposure to niclosamide, the active ingredient in the widely used molluscicide Bayluscide. PLoS Negl Trop Dis 9(10):e0004131

    PubMed  PubMed Central  Google Scholar 

  • Zhang L, Li L, Guo X et al (2015b) Massive expansion and functional divergence of innate immune genes in a protostome. Sci Rep 5:8693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S-M, Loker ES, Sullivan JT (2016) Pathogen-associated molecular patterns activate expression of genes involved in cell proliferation, immunity and detoxification in the amebocyte-producing organ of the snail Biomphalaria glabrata. Dev Comp Immunol 56:25–36

    PubMed  Google Scholar 

  • Zhong J, Wang W, Yang X et al (2013) A novel cysteine-rich antimicrobial peptide from the mucus of the snail of Achatina fulica. Peptides 39:1–5

    CAS  PubMed  Google Scholar 

  • Zhuang J, Cai G, Lin Q et al (2010) A bacteriophage-related chimeric marine virus infecting abalone. PLoS One 5(11):e13850

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We wish to thank Ms. Anne Rice for her superb and timely editorial assistance in compiling this manuscript. The ideas laid out in this chapter have been conceived, in large part, on account of works published by others, who are too numerous to mention individually; their papers are cited within. CJB was supported by NIH grant AI109134 and the Department of Integrative Biology at Oregon State University. ESL was supported by NIH grant AI101438 and the COBRE Center for Evolutionary and Theoretical Immunology (CETI), which is supported by NIH grant P30GM110907 from the National Institute of General Medical Sciences (NIGMS).

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Loker, E.S., Bayne, C.J. (2018). Molluscan Immunobiology: Challenges in the Anthropocene Epoch. In: Cooper, E. (eds) Advances in Comparative Immunology. Springer, Cham. https://doi.org/10.1007/978-3-319-76768-0_12

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