The gastropod foregut — evolution viewed through a developmental lens

Abstract

Comparative data on the developing gastropod foregut suggest that this multicomponent feeding complex consists of two developmental modules. Modularity is revealed by delayed development of the buccal cavity and radular sac (“ventral module”) relative to the dorsal food channel (“dorsal module”) in gastropods with feeding larvae compared with those that may have never had a feeding larval stage. If nonfeeding larvae like those of extant patellogastropods and vetigastropods are ancestral for gastropods, then the uncoupling and heterochronic offset of dorsal and ventral foregut modules allowed the post-metamorphic dorsal food channel to be co-opted as a simple but functional esophagus for feeding larvae. Furthermore, by reducing energy cost per ovum, the heterochronic offset may have given mothers the evolutionary option of increasing fecundity or investing in protective egg encapsulation material. A second developmental innovation was spatial separation of the dorsal and ventral foregut modules, as illustrated by distal foregut development in buccinid neogastropods and venom gland development in cone snails. Spatial uncoupling may have enhanced the evolvability of gastropod foreguts by allowing phenotypic variants of ventral module components to be selected within post-metamorphic ecological settings, without needing to be first tested for compatibility with larval feeding. Finally, we describe a case in which foregut modularity has helped facilitate a highly derived life history in which encapsulated embryos ingest nurse eggs.

Novel Genes, Ancient Genes, and Gene Co-Option Contributed to the Genetic Basis of the Radula, a Molluscan Innovation

“…The radula develops as a ventral outpocketing of the foregut ( Page 2002 ; Page and Hookham 2017 ) and is usually made up of numerous rows of teeth, which are situated on a cuticular ribbon, the radular membrane ( Runham 1963 ; Kerth 1973 ; Wiesel and Peters 1978 ; Mackenstedt and Märkel 1987) . Since the radula is worn down anteriorly, it is continuously produced by the odontoblast cell group, which is situated at the caudal end of the radular sack ( Runham 1963 ; Kerth 1973 ; Wiesel and Peters 1978 ; Mackenstedt and Märkel 1987) .…”

Insights into the Evolution of Shells and Love Darts of Land Snails Revealed from Their Matrix Proteins

“…For instance, the radula, or the chitinous teeth for feeding, was acquired in the last common ancestor of molluscs and was lost in bivalves. Interestingly, some genes that are expressed in the radula-forming region (ventral outpocketing of the foregut) (Page 2002; Page and Hookham 2017) are shared with genes related to other hard tissues (chaetae, spicules, and shells) in Lophotrochozoa (Hilgers et al. 2018).…”

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

“…It has long been known that much of the postmetamorphic buccal mass of gastropods, achieves an advanced state of differentiation prior to metamorphosis. In caenogastropods with planktotrophic larvae, some or all of the ciliated cells forming the distal larval esophagus are dissociated and ingested at metamorphosis (reviewed by Page & Hookham, ). Similarly, we speculate that much of the distal larval esophagus of S. denticulata is also destroyed at metamorphosis, because the mouth of animals sectioned at 2 days after metamorphosis led directly into a cuticle‐lined oral tube, which in turn led into a cuticle‐lined buccal cavity.…”