A novel three-part pharynx and its parallel evolution within symbiotic marine nematodes (Desmodoroidea, Stilbonematinae)

Abstract

Stilbonematinae are nematodes commonly found in shallow marine sands. They are overgrown by a genus- and species-specific coat of chemoautotrophic sulphur-oxidizing ectosymbiotic bacteria which profit from the vertical migration of their hosts through the chemocline by alternately gaining access to oxidizing and reducing chemical species, while in return, the host feeds on its symbionts. The subfamily exhibits a large morphological variability; e.g. the anterior pharynx is cylindrical in genera possessing a voluminous coat, but species with a bacterial monolayer possess a distinctly swollen corpus and therefore a tripartite pharynx. Since 18S-based phylogenetic analyses do not show close relationships between corpus-bearing species, we investigated the pharynx morphology using phalloidin staining in combination with confocal laser scanning microscopy, transmission electron microscopy and light microscopy in order to assess an independent evolution. The class-wide stable position of the subventral pharynx ampullae was used as a morphological marker. Ampullae are positioned at the anterior-most end of the isthmus in Cyathorobbea, further posterior in Catanema and Robbea and inside the corpus in Laxus oneistus. We therefore conclude an independent evolution of corpus enlargements within Stilbonematinae. This further suggests that pharynx morphology is driven by the volume of the symbiotic bacterial coat rather than phylogeny. Based on an existing mathematical model, an enlarged corpus should enable its bearer to ingest food in smaller quantities, in gourmet style, whereas a cylindrical pharynx would restrict its bearer to ancestral gourmand feeding. A review of pharynx types of Nematoda showed that the Stilbonematinae pharynx is substantially different compared to other tripartite pharynges. The lack of pharyngeal tubes and valves, the undivided corpus and evenly distributed nuclei in the isthmus warrant the definition of the “stilbonematoid” three-part pharynx.