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.
ABSTRACT The traits defining organismal body plans are expected to acquire burden, approaching invariance as they accumulate characters that depend on them, developmentally and functionally. Thus, the oldest features of a clade's body plan should decline in evolvability over time. With over 500 million years of evolutionary history, starting in the Cambrian Explosion of animal body plans, the marine bivalves are an ideal testing ground to evaluate the role of burden in macroevolution. We find substantial evolutionary changes in the novel elements constituting the foundation of the bivalve body plan—the ligament, hinge, and musculature that form the lever system that operates the animal's two shell valves. We observe instances of remodeling, translocation, and loss in each of these foundational structures of the bivalve body plan, and in the mineralized shell inherited from deeper ancestors. Our temporal inventory of these changes to the lever components and to the shell itself, including striking divergences from the ancestral bilateral symmetry, indicates that, contrary to expectations of burden increasing through time, most were not confined to the early evolutionary history of the class. Thus, despite their antiquity, these fundamental elements of the bivalve body plan have been surprisingly evolvable and remain so to the present day, underscoring a need to investigate these macroevolutionary outcomes in explicit developmental terms.
