Development of foregut and proboscis in the buccinid neogastropod Nassarius mendicus: Evolutionary opportunity exploited by a developmental module

Abstract

This article extends previous descriptions of foregut development and metamorphosis in neogastropods by providing data on the buccinid Nassarius mendicus, a species with a feeding larva. Histological sections showed that, like many other gastropods, the postmetamorphic buccal cavity and radular sac of N. mendicus differentiate during the larval stage from a ventral outpocketing of the distal larval esophagus. However, in N. mendicus the outpocketing also gives rise to the entire anterior esophagus and valve of Leiblein, suggesting that both these structures may be evolutionary derivatives of the gastropod buccal cavity. Scanning electron microscopy and three-dimensional reconstructions of section profiles revealed that the distal larval esophagus and larval mouth are completely destroyed at metamorphosis. The postmetamorphic mouth is formed as a new orifice. Furthermore, epithelia covering the proboscis and proboscis sac arise from preexisting epidermal epithelium of the larval head, an interpretation that contradicts an earlier suggestion on the origin of these epithelial elements in neogastropods with a feeding larval stage. These results, when compared to foregut development in other gastropods, lead me to propose that the gastropod buccal cavity and buccal mass is a developmental module. Canalized development of this module may have been important to the "evolvability" of the complex gastropod foregut, because it allowed a silent developmental novelty to arise (secondary formation of the postmetamorphic mouth) without disrupting development of the whole module. Nevertheless, this silent novelty might have subsequently facilitated dramatic evolutionary change by allowing the elaborate foregut structure of predatory, postmetamorphic neogastropods to arise in late stage larvae without compromising larval feeding.

How did phytoplankton-feeding larvae re-evolve within muricid gastropods? A view from developmental morphology

“…d Right lateral view of foregut immediately after loss of velar lobes showing almost complete loss of ciliated tube (ct). ae anterior esophagus, bc buccal cavity, ct ciliated tube, gL gland of Leiblein, me middle esophagus, p proboscis, pe posterior esophagus, rs radular sac, t tentacle, vl velar lobe, vL valve of Leiblein destroyed at metamorphosis (Page 2005(Page , 2011. Nevertheless, if the larval esophagus is no longer formed during muricid embryogenesis, then its loss is difficult to reconcile with the apparent re-emergence of swimming, phytoplankton-feeding larvae within this family.…”

“…Furthermore, the "ciliated tube" in the developing nucellids that we studied and the larval esophagus of previously studied planktotrophic caenogastropod larvae share a similar sequence of developmental transformations. Specifically, the ventral wall of the ciliated tube/larval esophagus of all these species incorporates a nest of stem cells that gives rise to the post-metamorphic distal foregut, and the ciliated tube/larval esophagus is fully or partially disassembled by cell dissociation at the time of metamorphic loss of the velar lobes (Page and Pedersen 1998;Page 2000Page , 2002Page , 2005Page , 2011Parries and Page 2003).…”

“…At metamorphosis, the distal larval esophagus is destroyed by cell dissociation, the larval mouth is sealed shut, and the juvenile mouth is created de novo ( Fig. 1e) (Page 2000(Page , 2005.…”

Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

“…In the primitive condition, the radular apparatus is a ribbon of recurved teeth that rasps algae off substrates. Initial studies on the developing foregut of predatory gastropods with a feeding larva, such as the buccinid neogastropod Nassarius mendicus [25], have suggested that many derived features of the postmetamorphic foregut result from extensively modified development of the ventral module. Modifications of the ventral module can occur without interfering with transport of larval food via the ciliated channel of the dorsal module.…”

Developing Nervous Systems in Molluscs: Navigating the Twists and Turns of a Complex Life Cycle

“…The development of these muscles is thus illustrative of conflicting demands placed on the mollusc during metamorphosis. That is, the full development of adult mouth parts would disrupt larval feeding and must therefore be postponed until as late as possible before metamorphosis [Page, 2005;Evans et al, 2009]. At the same time, however, molluscs are freeliving during the entire process of metamorphosis and generally cannot survive long without feeding.…”