Foregut Development and Metamorphosis in a Pyramidellid Gastropod: Modularity and Constraint within a Complex Life Cycle.

Abstract

Pyramidellids are tiny ectoparasitic gastropods with highly derived feeding structures for piercing and sucking. We attempted to resolve homology controversies about unique pyramidellid feeding structures by examining foregut development through larval and metamorphic stages, using sections for light and electron microscopy. We anticipated that, like many marine invertebrate larvae, post-metamorphic structures would differentiate extensively in late larvae to speed metamorphic transition. Previous studies of gastropods suggested that development of juvenile feeding structures in larvae was facilitated by foregut subdivision into dorsal and ventral developmental modules, and spatial uncoupling of these modules may have facilitated adaptive radiation in neogastropods. Observations of Odostomia tenuisculpta suggested that the stylet may be derived from cuticle-secreting buccal epithelium surrounding the proximal end of the salivary duct, whereas the stylet sheath could be either a derived jaw or a radular tooth. The anterior half of the remarkable buccal pump of these euthyneuran gastropods develops from the larval esophagus, which is unorthodox compared to caenogastropods, where extensive post-metamorphic specialization of a dorsal module component has not been previously described. The introvert tube develops from pouches of the distal larval esophagus and may actually be an eversible oral tube rather than an acrembolic proboscis. Minimal differentiation of presumptive juvenile foregut structures occurred during the larval stage of O. tenuisculpta, when compared to other gastropods. The stylet, stylet sheath, and buccal pump may be incompatible with functioning of the larval esophagus; thus, an explosive period of morphogenesis is necessary at metamorphosis. Although dorsal and ventral modules were recognizable during the development of O. tenuisculpta, we failed to find evidence that this modularity facilitated the extreme evolutionary remodeling of post-metamorphic feeding structures.