Functional morphology and evolutionary origin of the three-part pharynx in nematodes

The distinct morphological regions of the typical tripartite pharynx found in the nematode taxon Secernentea have distinctive functions. Besides the basic functions of sucking and pumping food against the pressure in the body cavity, the pharynx of Secernentea such as rhabditids serves two additional functions restricted to two pharyngeal subunits. The corpus traps bacteria behind the stoma and at its posterior end. The newly discovered pharyngeal pocket valve helps to trap particles behind the corpus in the rhabditid Poikilolaimus oxycercus and the cephalobid Acrobeles ciliatus (both Secernentea). The grinder of the terminal bulb serves for chewing trapped bacteria. The separated sites of trapping and chewing are connected by the isthmus that transports bacteria towards the grinder. It is likely that this complex feeding structure originated step by step from a two-part pharynx comprising a propharynx and the terminal bulb as in "Plectidae" (that probably include the closest relatives of the Secernentea within the "Adenophorea"). Analysis of video sequences of feeding rhabditids and plectids provided new data to reconstruct this transformation. Within the "Plectidae" two types of grinders occur. The first type or "parietinus type" has triangular chewing plates that can bulge medially and crush food particles. When they retract, new ingested particles are drawn into the grinder. The second type with more solid chewing plates called "butterfly valves" occurs in Ceratoplectus, Plectus parvus, and Wilsonema and can be homologized with the grinder in Secernentea ("Plectidae" is a paraphyletic taxon). Because butterfly valves cannot be retracted, the evolution of such valves required the evolution of an alternative mechanism to fill the grinder with bacteria. The differentiated closing pattern of the dilated pharynx lumen in Ceratoplectus, Plectus parvus, and Wilsonema can be interpreted as the first step in the development of a functional separation of trapping bacteria and of transporting them towards the grinder, which led to the morphologically discernible units of corpus and isthmus found in the Secernentea.