Cephalopod Neurogenomics

For more than 70 years cephalopod molluscs have served as powerful model organisms for comparative biology and neuroscience in particular. They represent a broad spectrum of complexity in their neuronal organizations: from relatively simple nervous systems in Nautilus to one of the most complex brains in the animal kingdom such as in Octopus. However, a major limitation in the field has been the lack of genomic information. As the initial steps in this direction, we have sequenced neuronal transcriptomes from key model cephalopod molluscs Nautilus, Loligo, Sepia and Octopus and compared them to neuronal transcriptomes of more than a dozen gastropod species and the sequenced Aplysia genome. Here, we will present a comparative analysis of these transcriptomes. First, this approach allowed us to identify both evolutionarily conserved neuronal genes and numerous genomic innovations within the phylum Mollusca, including novel genes encoding signal molecules such as prohormones and components of developmental programs. Molluscs have relatively slow evolving genomes allowing us to reveal numerous examples of extensive gene loss and gain across animal phyla (primarily associated with immunity, development and neuronal functions). Second, we have implemented several novel approaches that allowed us to characterize more than 50 fast and slow evolving neuropeptides relevant to locomotion, feeding, and defensive neural circuits. However, the phylum-scale comparative analysis indicates that neuropeptides are amongst the fastest evolving intercellular signal molecules. Third, using in situ hybridization we validated expression of more than dozen of identified neuropeptides (e.g. Betsin, Achatin, Sensorin and Pedal Peptides) supporting enormous expansion of neural cell lineages in cephalopods. Finally, using our transcriptome data and emerging phylogenomic approaches, we also were able to reconstruct the molluscan phylogeny and clarify the position of the phylum Cephalopoda as one of the ancient molluscan lineages. Combined comparative data from molluscs provides the unique opportunities to reconstruct ancestral neuronal lineages, identify cell homologies across species and reveal trends in evolution within neural circuits. Finally, the established molecular resources and the ability to map gene expression in a diversity of species should allow detailed study of a new hypothesis about independent origin of complex brains, and evolution of various biochemical, developmental and neuronal systems as well as provide a critical bridge between genes, circuits and behavior in the broad evolutionary context.