We are intrigued by one of the remaining great mysteries in animal evolution: how did our central nervous system (CNS) come into existence? What did it look like at first and how did it function? We are especially interested in the CNS of an extinct animal known as Urbilateria, the last common ancestor of humans, flies and most other ‘higher’ animals that live today, which lived some 600 million years ago in the ocean.
We have therefore chosen to work on a ‘living fossil’, the marine annelid Platynereis dumerilii, that we keep in laboratory culture. This species exhibits many ancient features in its lifestyle, anatomy and development. In bioinformatics comparisons we found that Platynereis also shows an ancestral gene inventory and gene structure.
We combine morphological and molecular approaches in a novel evo-devo approach, the molecular comparison of cell types. Animal nervous systems are made up of different sorts of sensory neurons, motor- and interneurons. Each type displays a characteristic ‘molecular fingerprint’, a unique combination of specifying transcription factors and downstream effector genes such as receptors, transmitters or neuropeptides. The comparison of molecular fingerprints allows the tracing of cell types through animal evolution. For example, in the Platynereis brain we have characterised a special type of photoreceptor cell, a ‘ciliary photoreceptor’ that by molecular fingerprint comparison relates to the rods and cones, the visual photoreceptors of the vertebrate retina. This has led to the fascinating hypothesis that the vertebrate eye evolved from within the Urbilaterian brain.
Besides ciliary photoreceptors, the Platynereis brain harbours several neuron types that have a dual function: they are both sensory and neurosecretory. The ongoing molecular characterisation of these cell types again revealed striking parallels to vertebrate cell types, mostly situated in the hypothalamus. Finally, we have also characterised the molecular architecture of the Platynereis trunk central nervous system and discovered striking parallels to the molecular architecture of the vertebrate neural tube. Basically, it appears that the vertebrate neural tube has evolved by the infolding of a pre-existing central nervous system that was in place already in the bilaterian ancestors.
Finally, we have also established neurobiological assay systems for larval swimming and for adult learning, combined with computer modelling of these and of other complex behavioural traits, in order to investigate the functions of conserved cell type and to gain insight into the neurobiology of marine planktonic life.
It is now clear that our molecular fingerprint comparisons between annelid,vertebrate and insect have the potential to unravel the origin of the bilaterian central nervous system. We are excited by the prospect of further deciphering the evolution of photoreceptor cells and of the diverse eye types that exist in animals. Also, we want to know the evolutionary origin of the most advanced brain part that ever evolved, the telencephalon. We have discovered neurons in Platynereis related to telencephalic neurontypes by molecular fingerprint, and started to investigate them further.
The clear picture is emerging that the Platynereis brain harbours many cell types so far known only for the vertebrates, but in a much more simple, very different overall arrangement. This makes it an attractive goal to elucidate the functioning of these cell types in the ancient marine environment in order to gain insight into the evolutionary origins of the vertebrate brain.