The other gastropod larvae: Larval morphogenesis in a marine neritimorph

Abstract

Two of the three major gastropod clades with feeding larvae are sister groups and larval morphogenesis for members of these clades, the Caenogastropoda and Heterobranchia, has been well studied. The third clade, the Neritimorpha, has an unstable phylogenetic position and little is known about development of their planktotrophic larvae. Information about larval morphology of neritimorphs and resolution of their controversial phylogenetic placement is critically important for understanding evolution of larval feeding within the Gastropoda. We describe larval morphogenesis to metamorphic competence for laboratory-reared larvae of Nerita melanotragus (Smith, 1884) (Neritimorpha: Neritidae). Preliminary observations suggest that prehatch larvae are capable of delayed hatching, possibly by entering a diapause state. Our description of larval morphogenesis, as based on tissue sections for light and transmission electron microscopy, scanning electron microscopy, three-dimensional-reconstructions of sectioned tissue, and labeling of muscles with fluorphore-tagged phalloidin, revealed four features that are unprecedented among both feeding and nonfeeding gastropod larvae. Larvae of N. melanotragus have muscles on the left and right side that both meet current criteria of a larval retractor muscle; shell-anchored muscles with oblique striations that project inside the visceral nerve loop to insert mainly on the velar lobes. They also have left and right digestive glands of similar size and a left and right hypobranchial gland. A larval "heart" is absent, but water circulation through the mantle cavity may be facilitated by large circular orifices, lined by patches of motile cilia, leading in and out of the mantle cavity. Comparison of larval traits among all three groups of gastropods with feeding larvae indicates that larvae of N. melanotragus have many unique characteristics, but they show more similarities to caenogastropod than to heterobranch larvae. These results are a significant step toward the goal of identifying primitive versus derived larval traits among feeding gastropod larvae.