Session 2: Evolution of the nervous system – evidence from non-bilateria and protostomia
Cnidaria and the emergence of neurogenesis
Professor Brigitte Galliot, University of Geneva, Switzerland
Hydra is a freshwater cnidarian polyp formed of two epithelial cell layers and three stem cell populations, equipped with a sophisticated apical nervous system that includes sensory-motor neurons, ganglia neurons and mechano-sensory cells named nematocytes. All these cells differentiate from interstitial stem cells, and are continuously replaced all along the life of the animals, highlighting the extreme dynamism of neurogenesis in Hydra. Previous studies also showed that animals easily survive the drug- or heatshock-induced elimination of interstitial stem cells that leave the epithelial cells unaffected. Several weeks later such Hydra become “epithelial”, i.e. have lost all their nerve cells, no longer react to touch nor catch their food, but surprisingly still regenerate after bisection, or bud when force-fed. However, Hydra oligactis that can undergo aging, rapidly loose de novo neurogenesis in this context, with dramatic impact on their neurological and developmental behaviours. To assess the role of adult de novo neurogenesis in the maintenance of fitness, regeneration and senescence, we performed quantitative RNAseq analysis on intact, heat-shocked, Hydroxyurea-treated or aging Hydra. We will present and discuss the obtained results in light of evolutionary considerations.
Dr Erich Jarvis, Duke University and Howard Hughes Medical Institute, USA
An option space for early neural evolution
Dr Gáspár Jékely, Max Planck Institute for Developmental Biology, Germany
The origin of nervous systems has traditionally been discussed within two conceptual frameworks. Input-output models stress the sensory-motor aspects of nervous systems, while internal coordination models emphasise the role of nervous systems in coordinating large-scale body movements. Here we consider both frameworks and apply them to describe aspects of each of three main groups of phenomena that nervous systems control: behaviour, physiology and development. We argue that both frameworks and all three aspects of nervous system function need to be considered for a comprehensive discussion of nervous system origins. This broad mapping of the option space enables a more comprehensive overview of the many influences and constraints that may have played a role in the evolution of the first nervous systems.
Genomic bases of multiple origins and parallel evolution of neurons and synapses: insights from ctenophores and molluscs
Professor Leonid Moroz, University of Florida, USA
Advances in Omics and their implementations to basal metazoan clades (Ctenophora, Porifera, Placozoa, Cnidaria, Bilateria) resulted to revisions of the animal phylogeny and hypotheses of neural evolution. Our analysis suggests that both neurons and synapses evolved independently from different cell lineages recruiting the ancestral machinery for secretion and reception developed in early eukaryotes.
The first case is the independent origin of neurons in ctenophores as evidenced by our combined genomic, proteomic, metabolomics and physiological studies on four ctenophore species (Pleurobrachia, Mnemiopsis, Bolinopsis and Beroe). Historically, temporal differentiation of cellular phenotypes found in unicellular eukaryotes (as result of their complex life cycles) was substituted and extended by spatial differentiation in metazoans leading to a greater diversity of cell types. Some components of synaptic and neuronal machinery might represent examples of convergent evolution.
The second remarkable example is the parallel origins of cell lineages supporting intercellular signaling using various transmitters. Combining data from 10+ phyla, including single-neuron RNA-seq and, unbiased single-cell epigenomic profiling, we will discuss how recruitment of various molecular modules together with environmental constrains might lead to independent origins of neurons and synapses across distinct animal clades.
Phylogenetic reconstructions also suggest that neuronal centralisation and mosaic formation of complex brains evolved at least 12 times across the animal kingdom, with 5 independent centralisation events in the molluscan clade including cephalopods - the ‘primates of the sea’. Thus, we define neurons as a functional rather than a genetic category. Neurons are polarised secretory cells specialised for directional propagation of electrical signals leading to release of intracellular messengers – features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbours without affecting all intervening cells en route. However, using an array of molecular markers within some animal lineages, especially in molluscs, one can recognise homologous neuronal lineages. These examples and criteria for homologisation of distinct cell lineages will be discussed toward reconstruction of natural classification of neurons or NeuroSystematics.
Where is my mind? How sponges and placozoans may have lost neural cell types
Dr Joseph Ryan, University of Florida, USA
For over 150 years, it was thought that sponges were the sister group to all other animals (if they were animals at all) and that the sponge body plan represented a primitive stage in animal evolution. Similarly, it has long been thought that placozoans represent a basic body type that has endured hundreds of million years of evolution. Recent phylogenetic analyses of animal genomes and transcriptomes, however, have challenged these ideas, suggesting that ctenophores are the sister group to all other animals and implying that sophisticated cell types like neurons either evolved multiple times or were lost during the evolution of sponges and placozoans. Thus far, the far more preferred hypothesis appears to be that neural cell types evolved multiple times. I argue that historical bias may be playing a role in the rejection of cell-type loss as an explanation of the data, and that a novel analysis of evidence in light of this hypothesis is both compelling and revealing.
Development and structure of anthozoan nervous systems
Professor Ulrich Technau, University of Vienna, Austria
Cnidarians are the sister group of Bilateria and can therefore provide important insights into the evolution of key bilaterian traits. One of the hallmarks of bilaterians is the central nervous system. Cnidarians do not possess a central nervous system or a brain, and the nervous system of cnidarians has often been referred to as "diffuse". However, regional accumulations of neurons or nerve rings for instance found at the margin of jellyfish, as well as patterning of specific neuronal subtypes expressing different neurotransmitters suggest a certain level of complexity. Neurogenesis has been mainly studied in the hydrozoan Hydra and in the sea anemone Nematostella vectensis. While in Hydra, neurons arise from multipotent interstitial stem cells, such stem cells have not been found in Nematostella. Instead, in this organism neurons appear to differentiate directly from epithelial cells. I will discuss the similarities and differences of nervous system formation in the context of patterning of the body plan and compare it with bilaterians.