Development and evolution of adult feeding structures in Caenogastropods: overcoming larval functional constraints

Comparative study of the developing foregut in three species of caenogastropods, including an herbivorous grazer (Lacuna vincta) and two carnivores (Euspira [Polinices] lewisii and Nassarius mendicus), suggests how the specialized adult foregut of a carnivorous neogastropod evolved within a life cycle having a planktotrophic larva. Postmetamorphic feeding structures (buccal cavity and radular sac) in all three species achieve advanced differentiation in the larval stage, permitting juvenile feeding at 3 days postmetamorphosis. Recent phylogenetic hypotheses for the Gastropoda predict that foregut developmental patterns in E. lewisii and N. mendicus are derived, relative to that of L. vincta. In hatching larvae of these three, the anlage of postmetamorphic feeding structures is a small patch of nonciliated cells embedded in the ventral wall of the larval foregut and the patch soon forms an outpocketing. During subsequent morphogenesis, Euspira lewisii and N. mendicus share a developmental novelty that involves semi-isolation of the developing, postmetamorphic buccal cavity and radular sac from the larval foregut and formation of a new, definitive mouth at metamorphosis. Nassarius mendicus, a neogastropod, embellishes this novelty by adding the entire anterior esophagus and valve of Leiblein (de novo structures) to the semi-isolated buccal cavity. Therefore, a valve and long stretch of muscular anterior esophagus, which are necessary for feeding with a pleurembolic proboscis, are preformed in the larval stage of this neogastropod without interfering with larval feeding. The inferred evolutionary events leading to postmetamorphic feeding specialization in N. mendicus are invisible in adults; they require reconstruction from comparative developmental analysis.