Comparative analysis of the tardigrade feeding apparatus: adaptive convergence and evolutionary pattern of the piercing stylet system

A thorough analysis of the cuticular parts of tardigrade feeding apparatuses was performed in order to provide a more complete understanding of their evolution and their potential homologies with other animal phyla (e.g. Cycloneuralia and Arthropoda). The buccal- pharyngeal apparatuses of eight species belonging to both Eutardigrada and Heterotardigrada were studied using light and scanning electron microscopy. This study supports and completes a previous study on the relationships between form and function in the buccalpharyngeal apparatus of eutardigrades. The common sclerified structures of the tardigrade buccal-pharyngeal apparatus are: a buccal ring connected to a straight buccal tube, a buccal crown, longitudinal thickenings within the pharynx, and a stylet system composed of piercing stylets within stylet coats, and stylet supports. Specifically, heterotardigrades (Echiniscoidea) have a narrow buccal tube; long piercing stylets, each with a longitudinal groove, that cross one another before exiting the mouth; pharyngeal bars and secondary longitudinal thickenings within the pharynx. In contrast, eutardigrades have stylets which are shorter than the buccal tube; Parachela have pharyngeal apophyses and placoids within the pharynx, while Apochela lack a buccal crown and cuticular thickenings within the pharynx, the buccal tube is very wide, and the short stylets are associated with triangular-shaped stylet supports. In both classes, when the piercing stylet tips emerge from the mouth to pierce food, the buccal tube opening is almost completely obstructed, which may hinder food uptake. In heterotardigrades, the crossing of the piercing stylets may further decrease food uptake, however this disadvantage may have been reduced in echiniscids by the evolution of a long buccal tube and long stylets able to run more parallel to the buccal tube. In contrast, eutardigrades evolved different strategies. In the order Apochela and in several Itaquasconinae (Parachela), the buccal tube is wide, the stylets are short and run parallel to the tube without crossing. In other Parachela, the piercing stylets do not cross one another because they are curved. Further, the development of an anterior bend in the buccal tube (e.g. in Doryphoribius and Macrobiotoidea) may allow the shift of the stylet sheaths to a more ventral position so that a wide portion of the mouth is free during the piercing stylet movements. The possible convergent evolution of several structures of the buccal-pharyngeal apparatus (e.g. ventral lamina, pharyngeal tube, wide buccal tube without buccal crown, buccal lamellae) was analysed and discussed.