Salivary Glands in Predatory Mollusks: Evolutionary Considerations

Many marine mollusks attain or increase their predatory efficiency using complex chemical secretions, which are often produced and delivered through specialized anatomical structures of the foregut. The secretions produced in venom glands of Conus snails and allies have been extensively studied, revealing an amazing chemical diversity of small, highly constrained neuropeptides, whose characterization led to significant pharmacological developments. Conversely, salivary glands, the other main secretory structures of molluscan foregut, have been neglected despite their shared occurrence in the two lineages including predatory members: Gastropoda and Cephalopoda. Over the last few years, the interest for the chemistry of salivary mixtures increased based on their potential biomedical applications. Recent investigation with -omics technologies are complementing the classical biochemical descriptions, that date back to the 1950s, highlighting the high level of diversification of salivary secretions in predatory mollusks, and suggesting they can be regarded as a pharmaceutical cornucopia. As with other animal venoms, some of the salivary toxins are reported to target, for example, sodium and/or potassium ion channels or receptors and transporters for neurotransmitters such as, glutamate, serotonin, neurotensin, and noradrenaline, thus manipulating the neuromuscular system of the preys. Other bioactive components possess anticoagulant, anesthetic and hypotensive activities. Here, we overview available knowledge on the salivary glands of key predatory molluscan taxa, gastropods, and cephalopods, summarizing their anatomical, physiological and biochemical complexity in order to facilitate future comparative studies on main evolutionary trends and functional convergence in the acquisition of successful predatory strategies.

[1]  J. Rhee,et al.  Transcriptome profiling suggests roles of innate immunity and digestion metabolism in purplish Washington clam , 2018, Genes & Genomics.

[2]  D. Craik,et al.  Bioactive Compounds Isolated from Neglected Predatory Marine Gastropods , 2018, Marine drugs.

[3]  Y. Kantor,et al.  Morphology of the anterior digestive system of tonnoideans (Gastropoda: Caenogastropoda) with an emphasis on the foregut glands , 2016 .

[4]  M. Oliverio,et al.  The venomous cocktail of the vampire snail Colubraria reticulata (Mollusca, Gastropoda) , 2015, BMC Genomics.

[5]  D. Lindberg,et al.  Consensus and Confusion in Molluscan Trees: Evaluating Morphological and Molecular Phylogenies , 2014, Systematic biology.

[6]  G. Fiorito,et al.  Immunohistochemical Analysis of Neuronal Networks in the Nervous System of Octopus vulgaris , 2015 .

[7]  Nicholas R Casewell,et al.  Complex cocktails: the evolutionary novelty of venoms. , 2013, Trends in ecology & evolution.

[8]  A. Antunes,et al.  Molecular Phylogeny and Evolution of the Proteins Encoded by Coleoid (Cuttlefish, Octopus, and Squid) Posterior Venom Glands , 2013, Journal of Molecular Evolution.

[9]  Stephen A. Smith,et al.  Resolving the evolutionary relationships of molluscs with phylogenomic tools , 2011, Nature.

[10]  J. Vinther,et al.  Cephalopod origin and evolution: A congruent picture emerging from fossils, development and molecules , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[11]  M. Raats,et al.  The role of consumers. , 2010, Nestle Nutrition workshop series. Paediatric programme.

[12]  M. V. Modica,et al.  The Neogastropoda: Evolutionary Innovations of Predatory Marine Snails with Remarkable Pharmacological Potential , 2010 .

[13]  R. Norton,et al.  The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. , 2009, Annual review of genomics and human genetics.

[14]  J. Norman,et al.  Tentacles of Venom: Toxic Protein Convergence in the Kingdom Animalia , 2009, Journal of Molecular Evolution.

[15]  G. Bigatti,et al.  Feeding behavior of Adelomelon ancilla (Lighfoot, 1786): A predatory neogastropod (Gastropoda: Volutidae) in Patagonian benthic communities , 2009 .

[16]  M. Ishida,et al.  Purification and molecular cloning of SE-cephalotoxin, a novel proteinaceous toxin from the posterior salivary gland of cuttlefish Sepia esculenta. , 2008, Toxicon : official journal of the International Society on Toxinology.

[17]  J. Biggs,et al.  Alpha-conopeptides specifically expressed in the salivary gland of Conus pulicarius. , 2008, Toxicon : official journal of the International Society on Toxinology.

[18]  D. Mebs,et al.  Distribution of tetrodotoxin in the body of the blue-ringed octopus (Hapalochlaena maculosa). , 2007, Toxicon : official journal of the International Society on Toxinology.

[19]  H. Weber Der Darm von Dolium galea l, eine vergleichend anatomische untersuchung unter besonderer berücksichtigung der tritonium-arten , 1927, Zeitschrift für Morphologie und Ökologie der Tiere.

[20]  A. Kanda,et al.  Isolation and characterization of novel tachykinins from the posterior salivary gland of the common octopus Octopus vulgaris , 2003, Peptides.

[21]  A. Power,et al.  The seasonality and role of the neurotoxin tetramine in the salivary glands of the red whelk Neptunea antiqua (L.). , 2002, Toxicon : official journal of the International Society on Toxinology.

[22]  Alexandre Pouget,et al.  Computational approaches to sensorimotor transformations , 2000, Nature Neuroscience.

[23]  J. Castro,et al.  Evidence of external digestion of crustaceans in Octopus vulgaris paralarvae , 2000, Journal of the Marine Biological Association of the United Kingdom.

[24]  L. Page Development and evolution of adult feeding structures in Caenogastropods: overcoming larval functional constraints , 2000, Evolution & development.

[25]  A. Page,et al.  The Fine Structure and Function of the Anterior Foregut Glands of Cymatium Intermedius (Cassoidea: Ranellidae) , 1999 .

[26]  M. Thorndyke,et al.  Presence of a toxin in the salivary glands of the marine snail Cymatium intermedius that targets nicotinic acetylcholine receptors , 1998 .

[27]  K. Elekes Cephalopod Behaviour , 1997, Acta Biologica Hungarica.

[28]  Y. Nagashima,et al.  Toxins in the salivary gland of some marine carnivorous gastropods , 1994 .

[29]  M. S. Grisley Separation and partial characterization of salivary enzymes expressed during prey handling in the octopus eledone cirrhosa , 1993 .

[30]  E. B. Andrews The fine structure and function of the salivary glands of Nucella lapillus (Gastropoda: Muricidae) , 1991 .

[31]  M. Elphick,et al.  Pharmacologically active constituents of the accessory salivary and hypobranchial glands of Nucella lapillus , 1991 .

[32]  P. Boyle,et al.  Chitinase, a new enzyme in octopus saliva , 1990 .

[33]  I. Gould,et al.  Food poisoning due to the consumption of red whelks (Neptunea antiqua) , 1988, Epidemiology and Infection.

[34]  F. Minniti Morphological and histochemical study of pharynx of Leiblein, salivary glands and gland of Leiblein in the carnivorous gastropoda Amyclina tinei Maravigna and Cyclope neritea Lamarck (Nassariidae: Prosobranchia stenoglossa) , 1986 .

[35]  B. Morton Prey Capture in Lyonsiella Formosa (Bivalvia: Anomalodesmata: Verticordiacea) , 1984 .

[36]  M. Nixon Is there external digestion by Octopus , 1984 .

[37]  A. Barber Nervous Control of the Salivary Glands of the Carnivorous Mollusc Philine Aperta , 1983 .

[38]  B. Morton Prey capture in the carnivorous septibranch Poromya granulata (Bivalvia:Anomalodesmata:Poromyacea) , 1981 .

[39]  M. R. Carriker Shell penetration and feeding by naticacean and muricacean predatory gastropods: a synthesis , 1981 .

[40]  C. House PHYSIOLOGY OF INVERTEBRATE SALIVARY GLANDS , 1980 .

[41]  John D. Taylor,et al.  Food specialization and the evolution of predatory prosobranch gastropods , 1980 .

[42]  G. Hemingway Evidence for a paralytic venom in the intertidal snail, Acanthina spirata (Neogastropoda: Thaisidae). , 1978, Comparative biochemistry and physiology. C: Comparative pharmacology.

[43]  G. Vermeij The Mesozoic marine revolution: evidence from snails, predators and grazers , 1977, Paleobiology.

[44]  L. Cariello,et al.  α-及びβ-セファロトキシン : Octopus vulgarisの後方だ液せんからの2つの麻ひたんぱく質 , 1977 .

[45]  L. Zanetti,et al.  α- and β-cephalotoxin: Two paralysing proteins from posterior salivary glands of Octopus vulgaris , 1977 .

[46]  L. Zanetti,et al.  Alpha- and beta-cephalotoxin: two paralysing proteins from posterior salivary glands of Octopus vulgaris. , 1977, Comparative biochemistry and physiology. C: Comparative pharmacology.

[47]  U. Lidman,et al.  Secretion of sulfuric acid in Cassidaria echinophora Lamarck (Mollusca: Mesogastropoda, marine carnivorous snail). , 1976, Comparative biochemistry and physiology. A, Comparative physiology.

[48]  L. Gianfreda,et al.  Cellulase and related enzyme activities in a carnivorous mollusc: Octopus vulgaris Lamarck. , 1975, Comparative biochemistry and physiology. B, Comparative biochemistry.

[49]  S. Philips,et al.  Tyramines inOctopus nerves , 1975, Brain Research.

[50]  B. Shapiro,et al.  Purification and composition of a toxin from the posterior salivary gland of Octopus dofleini. , 1974, Toxicon : official journal of the International Society on Toxinology.

[51]  W. F. Ponder The origin and evolution of the Neogastropoda. , 1973, Malacologia.

[52]  Ponder Wf The origin and evolution of the Neogastropoda. , 1973 .

[53]  G. N. Mir,et al.  Pharmacological investigation of salivary gland of Thais haemastoma (Clench). , 1972, Toxicon : official journal of the International Society on Toxinology.

[54]  P. Molinoff,et al.  Distribution of octopamine in nervous tissues of Octopus vulgaris. , 1971, British journal of pharmacology.

[55]  C. Fleming Case of poisoning from red whelk. , 1971, British medical journal.

[56]  V. Fretter,et al.  SOME ASPECTS OF THE FUNCTIONAL ANATOMY AND BIOLOGY OF CYMATIUM AND BURSA , 1969 .

[57]  E. D. Irvine Psychiatric Social Workers , 1968 .

[58]  J. Young The buccal nervous system of octopus , 1965, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[59]  V. Erspamer,et al.  Occurrence and some properties of eledoisin in extracts of posterior salivary glands of Eledone. , 1962, British journal of pharmacology and chemotherapy.

[60]  J. Mclean FEEDING BEHAVIOR OF THE CHITON PLACIPHORELLA , 1962 .

[61]  F. Ghiretti TOXICITY OF OCTOPUS SALIVA AGAINST CRUSTACEA * , 1960, Annals of the New York Academy of Sciences.

[62]  F. Ghiretti Cephalotoxin: the Crab-paralysing Agent of the Posterior Salivary Glands of Cephalopods , 1959, Nature.

[63]  R. Fänge,et al.  COMPARISON BETWEEN BIOLOGICAL EFFECTS OF NEURINE AND A SALIVARY GLAND EXTRACT OF NEPTUNEA ANTIQUA , 1958 .

[64]  S. Bianco Notizie biologiche riguardanti specialmente il periodo di maturità sessuale degli animali del golfo di Napoli , 1888 .

[65]  J. Young Cephalopoda , 1871, Transactions of the Glasgow Geological Society.