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Cellular innovation driving nervous system evolution

Periodic Reporting for period 4 - NeuralCellTypeEvo (Cellular innovation driving nervous system evolution)

Reporting period: 2022-12-01 to 2024-05-31

The evolutionary emergence of nervous systems is yet enigmatic, but has interested society since Greek philosophers started to contemplate human origins. The NeuralCellTypeEvo project investigates when and in what form the first nervous system emerged. For this, we aim to understand cell type evolution in animals. We trace how the multifunctional cells that were typical for early animals became distinct, by a step-wise process of cellular diversification involving division of labour and specialisation.
To gain insight into the evolution of neurons in animals, we have characterised all cells of the body in selected animals, which are important for tracing the evolutionary history of nervous systems. This includes looking at all genes that are differentially expressed between the cells, and also a description of cellular phenotypes by light and electron microscopy. In particular, we have characterised all cell types of a sponge, which do not have a nervous system. Here, we found cells expressing proteins that are known to play a role in nervous functions in other animals. For example, the stellar-shaped neuroid cells communicate with other sponge cells and may relate to cells from which the first neurons evolved (figure). Beyond that, we have characterised cell types including all neurons in a marine bristle worm and in a chiton, which have simple nervous systems that are informative about the origins of nervous system centralisation. This work has revealed specific neuron types in these animals that relate to neuron types in our body and are thus likely to have existed in the last common ancestor of all bilaterian animals. This includes neurons of sensory associative centres in the brain and also gut neurons. Finally, we have looked at the brains of lampreys and sharks, representing early-branching vertebrate groups. This part of the project has revealed ancient components of our forebrain and eyes, which allows us to reconstruct the path of evolution that led to the complex brain and eyes in the human body.
Looking at animal evolution at the cell type level, to understand how cells diversified and specialised on the multiple tasks that together form an animal, is a very new direction to which we have essentially contributed. With our project, we have shown ways how to characterise the entire complement of cell types for a whole animal; how to compare cell types between species; how to infer ancient paths of cell type evolution; and most important for our aim, characterise key steps in nervous system evolution, from the first neurons to nerve nets, centralisation, and the emergence of complex brains and eyes. With our cellular comparisons we have thus been able to suggest important parts of the nervous system that were likely already present in the last common ancestor of bilaterian animals. For example, this animal likely already possessed sensory-associative centres that later gave rise to our cortex, and motor and interneuron types that today exist in our spinal cord. We also unravelled the origins of our eyes, which can be traced back to a precursor organ that was already able to detect different wavelengths of light, most likely acting as a depth gauge for early swimming vertebrates, and which later split and evolved into the lateral eyes that we possess today and into the pineal organ, which controls our day-night rhythm and sleep.
Neuroid cell (violet) in a sponge choanocyte chamber (blue). Credit: Jacob Musser, Klaske Schippers.