Siphonariid development: Quintessential euthyneuran larva with a mantle fold innovation (Gastropoda; Panpulmonata)

• Published in: Journal of morphology (1931) 2019-05, Vol.280 (5), p.634-653
• Main Authors: Page, Louise R., Hildebrand, Ilsa M., Kempf, Stephen C.
• Format: Article
• Language: English
• Subjects: Animal Shells - anatomy & histology; Animal Shells - ultrastructure; Animals; Epithelium - anatomy & histology; Epithelium - ultrastructure; Euthyneura; evolvability; Gastrointestinal Tract - anatomy & histology; Gastrointestinal Tract - ultrastructure; Gastropoda - anatomy & histology; Gastropoda - classification; Gastropoda - growth & development; Gastropoda - ultrastructure; innovation; Larva - anatomy & histology; Larva - growth & development; metamorphosis; Morphogenesis; Osmoregulation; Phylogeny; planktotrophic larva; Sense Organs - anatomy & histology; Sense Organs - ultrastructure
• ISSN: 0362-2525; 1097-4687
• DOI: 10.1002/jmor.20971

Recent phylogenetic revisions of euthyneuran gastropods (“opisthobranchs” and “pulmonates”) suggest that clades with a planktotrophic larva, the ancestral life history for euthyneurans, are more widely distributed along the trunk of the euthyneuran tree than previously realized. There is some indication that the planktotrophic larva of euthyneurans has distinctive features, but information to date has come mainly from traditional “opisthobranch” groups. Much less is known about planktotrophic “pulmonate” larvae. If planktotrophic larvae of “pulmonates” share unique traits with those of “opisthobranchs,” then a distinctive euthyneuran larval‐type has been the developmental starting template for a spectacular amount of evolved morphological and ecological disparity among adult euthyneurans. We studied development of a siphonariid by preparing sections of larval and postmetamorphic stages for histological and ultrastructural analysis, together with 3D reconstructions and data from immunolabeling of the larval apical sensory organ. We also sought a developmental explanation for the unusual arrangement of shell‐attached, dorso‐ventral muscles relative to the mantle cavity of adult siphonariids. Adult siphonariids (“false limpets”) have a patelliform shell but their C‐shaped shell muscle partially embraces a central mantle cavity, which is different from the arrangement of these components in patellogastropods (“true limpets”). It is not obvious how shell muscles extending into the foot become placed anterior to the mantle cavity during siphonariid development from a veliger larva. We found that planktotrophic larvae of Siphonaria denticulata are extremely similar to previously described, planktotrophic “opisthobranch” larvae. To emphasize this point, we update a list of distinctive characteristics of planktotrophic euthyneuran larvae, which can anchor future studies on the impressive evolvability of this larval‐type. We also describe how premetamorphic and postmetamorphic morphogenesis of larval mantle fold tissue creates the unusual arrangement of shell‐muscles and mantle cavity in siphonariids. This result adds to the known postmetamorphic evolutionary innovations involving mantle fold tissue among euthyneurans. Traits of a siphonariid planktotrophic larva extend the known phylogenetic distribution of a distinctive larval‐type for many lineages of spectacularly diverse adult euthyneuran gastropods. Premetamorphic and postmetamorphic morphogenesis of the larva