Salivary Glands in Predatory Mollusks: Evolutionary Considerations

Abstract

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.

Anatomical and histochemical features of the digestive system ofOctopus vulgarisCuvier, 1797 with a special focus on secretory cells

“…Moreover, the posterior salivary glands in a number of cephalopod species have been found to contain various proteolytic enzymes that contribute to protein digestion (Grisley & Boyle, ; Mancuso, Giordano, Genovese, Denaro, & Caruso, ; Moroshita, Ueno, & Takahashi, ; Ponte & Modica, ). Our findings confirm the presence of serous cells in the oral cavity as previously described.…”

“…However, the glandular epithelia of the buccal mass and submandibular gland contain scarce granular cells and numerous mucous cells, suggesting specialisation of these tissues in mucus secretion. Early studies show evidences of the high diversification of salivary secretions, suggesting that the salivary gland may play different roles in feeding (see Ponte & Modica, ).…”

Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

“…However, it has not yet been possible to properly investigate the evolutionary history of these genes in cephalopods due to a lack of genome sequences for species known to produce tachykinin venom proteins. Additionally, there are few transcriptomes of cephalopod venom glands that can provide information on expression within the tissue . Despite this, a dynamic evolutionary picture is emerging, for example, a loss of tachykinin expression in the venom gland has been observed in the southern blue‐ringed octopus ( Hapalochlaena maculosa ) .…”

Bioactive Compounds Isolated from Neglected Predatory Marine Gastropods

“…Tetramine ( Figure 4 A) acts by blocking nicotinic acetylcholine receptors, but human food poisoning cases caused by ingesting these gastropods are fortunately not serious because this toxin is easily degraded or cleared [ 14 , 37 ]. Indeed, symptoms typically vanish within 24 h at most, with no long-term complications reported [ 41 , 42 ].…”

“…For example, while true venom glands are limited to (but not ubiquitous in) the superfamily Conoidea [ 11 ], some species from the Tonnoidea superfamily have indeed demonstrated the ability of their accessory salivary glands to function as ‘venom’ glands [ 3 , 12 ]. Most species of predatory gastropods in Tonnoidea have a large pair of salivary glands that are differentiated into anterior and posterior lobes, and are responsible for producing sulfuric acid (pH 2) [ 13 , 14 ].…”