Integrative developmental studies on basal molluscs

Molluscs exhibit a large variation of bodyplan morphologies that include millimetre-sized, worm-shaped, spicule- bearing "aplacophoran" groups (Solenogastres and Caudofoveata), eight-shelled polyplacophorans, bivalves, gastropods (snails and slugs), and cephalopods (nautiluses, squids, and octopuses). Despite recent technological progress in molecular and (micro-) morphological applications, the evolutionary emergence of the phylum Mollusca remains obscure. Questions whether or not molluscs are derived from a segmented ancestor (as the annelids) are still unresolved, and the discussion about their sister group is still ongoing. In order to shed light on these questions from a developmental perspective, we will investigate the ontogeny of nervous and muscle systems as well as the expression of "segmentation genes" in the Solenogastres, the recent group that is thought to bear most similarities with the last common ancestor to all molluscs. A recently established lab culture of four solenogaster species by one collaborator, Dr. Christiane Todt (University of Bergen), will provide us with the study material. Specific questions addressed include whether or not the expression patterns of the "segmentation genes" Notch, Delta, engrailed, wingless, and hedgehog bear any similarities to those of the segmented annelids and arthropods and/or what other functions these genes may have acquired during molluscan evolution. These studies will be performed on our model solenogaster species, Wirenia argentea. In addition, we will analyse neuro- and myogenesis in all four species with the aim to provide a model for the supposedly basal condition in Mollusca, and in order to test whether or not neural and/or muscular components in Solenogastres are formed in a strict anterior to posterior progression as in the segmented annelids. These data should provide us with in-depth insights into the basal neuromuscular and genetic toolkit of Mollusca and will allow us to propose an ancestral condition for these characters from which the other molluscan subtaxa derived. Moreover, the morphological data generated will provide potential insights into the phylogenetic relationships of Mollusca within Lophotrochozoa. In addition to that, the large EST dataset produced will provide an excellent data mining platform for future molecular analyses into the functions of numerous key developmental genes in basal molluscs, thus allowing for deductions concerning basal versus co-opted gene functions in the evolution of bodyplan novelties.

One of the key findings of the current project is that the worm-shaped group of mollusks with an extremely simple body plan, the Solenogastres, stem from an ancestor that was much more complex. Comparisons with the closely related polyplacophorans revealed a number of homologous muscular subsets in larvae of both animals. However, while they to a large extent survive metamorphosis and thus are retained in the adult body in polyplacophorans, they are mostly reduced or remodelled during solenogaster development. Therefore, the simple morphology of adult Solenogastres must be regarded a secondary condition that occurred in the course of evolution from a much more complex, polyplacophoran-like ancestor. These findings strikingly contradict current textbook knowledge that usually proposes a simple worm-like ancestor at the base of this group of mollusks. The second key finding is a confirmation of our earlier hypothesis that similar to all other mollusks no trace of ancestral segmentation is apparent during solenogaster ontogeny. Thus, the often proposed origin of Mollusca from a segmented ancestor can now be almost entirely ruled out, also because our data do confirm this on both morphogenetic (development of muscles and the nervous system) and molecular (gene expression) levels.