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

Abstract

Molluscs constitute a richly diversified phylum, containing abundant species that have successfully invaded a variety of habitats. Despite the long-standing importance of its various members as model species for neurobiology, research on the development of the molluscan nervous system has lagged behind that on several other phyla. Recent studies, however, have begun to sketch an overview of neural development during the complex life cycles of these animals, involving multiple larval and postlarval stages and often including processes of torsion and occasionally detorsion affecting the entire body plan. The first neurons appear early in life and innervate a variety of larval organs. The central and peripheral neurons that comprise the adult nervous system generally appear later in larval life. Metamorphosis involves the loss of many neurons and the gain of others, and yet more neurons change to accommodate transitions in modes of locomotion, feeding and habitat. But such large-scale transitions do not stop at metamorphosis as massive changes in body size and behavior occur during juvenile and adult stages, and the nervous system must change accordingly to meet the demands of expanding target tissues and the need to generate new behaviors. Work over the years has gradually revealed some of the genes important in molluscan neural development, but recent whole-genome, EST and microarray projects are now allowing much more rapid progress and providing a valuable molluscan perspective for understanding broader issues concerning the evolution of the nervous system across the animal kingdom.

A comprehensive fate map by intracellular injection of identified blastomeres in the marine polychaete Capitella teleta

“…In gastropod mollusks, the ganglia of the central nervous system arise later in larval development [36-38], making fate mapping technically challenging. The nemertean C. lacteus undergoes a radical metamorphosis, with the larval nervous system being entirely replaced by derivatives of imaginal discs.…”

“…In C. fornicata , 2b contributes to the supra-intestinal and sub-intestinal ganglia, and 2a and 2c contribute to the left and right pedal ganglia. Interestingly, 2d gives rise to the posterior mantle cell [10], which is one of the first neurons to differentiate, and its axons may serve as a scaffold for later central nervous system development [36,38]. Peripheral neurons in C. fornicata are generated by all 1q and 2q micromeres [10], whereas third quartet contributions to the nervous system have not yet been determined.…”

Phylogenomics meets neuroscience: How many times might complex brains have evolved?

“…Evidently, different neuronal lineages can be labeled by different molecular markers [12–14, 89–93] indicating that they might not be genealogically related, but instead form a bipartite brain with at least two distinct components [57, 58] or even more complex assembles with multiple distinct cell lineages.…”

Preface to Molluscan Neurobiology: Recent Advances and New Vistas

“…Although modern neuroscience methods obviate much of the need for working on giant neurons, there are lecular information. Two papers in this volume address those issues [Croll, 2009;Moroz, 2009].…”

“…In this volume, Croll [2009] provides a guide to the development of the molluscan nervous system, discussing in particular the organization of the larval nervous system and the metamorphosis into the adult nervous system. As noted in this article, the neurogenesis and patterning of the nervous system have not been studied as deeply in molluscs as in arthropods, nematodes, and mammals.…”