New Insight to Morphogenetic Movements Underlying Gastrulation in the Freshwater Gastropod Lymnaea stagnalis (Mollusca: Heterobranchia)

ABSTRACT

Gastropod molluscs, inhabiting marine, freshwater, and terrestrial environments, are a unique group to uncover the evolution of developmental pathways shaped by adaptation to novel environments. However, the detailed comparative data are available for a few marine gastropods only. We present here the first comprehensive, stage‐by‐stage description of early embryogenesis in a representative of freshwater gastropod molluscs. We visualized and characterized the cellular basis of morphogenetic movements in the pond snail Lymnaea stagnalis , from cleavage to late gastrula, using state‐of‐the‐art microscopy. We traced dpMAPK localization during 3D organizer differentiation and endomesoderm segregation. For the first time, rhythmic embryonic pulsations, potentially regulating development through biomechanical forces, were demonstrated for Spiralia. We revealed a continuous network of long filopodia connecting all embryonic cells throughout development, and speculate that they may function as cytonemes. This finding suggests a putative structural basis for cell−cell communication in Lymnaea . We also provide novel insights into the morphogenetic movements of gastropod gastrulation demonstrating that in Lymnaea the segregation and internalization of the two germ layers—mesoderm and endoderm—are separated in time. Gastrulation initiates at the 25‐cell stage and proceeds through three distinct phases: primary mesoderm formation; invagination of the vegetal plate composed of bottle‐shaped endodermal cells; shaping and zippering of the blastopore. Cellular mechanisms underlying the endoderm segregation contribute to the elongation of the embryo, the displacement of the mouth Anlage toward the ventral side, and the approximation of the animal and vegetal poles. Our data provides new material for establishing Lymnaea as a valuable model for cutting‐edge investigations in Evo‐Devo.