Back Through Time: How Cnidarians and Basal Metazoans Shed Light on Ancient Nervous Systems

Abstract

The origin of neurons and the evolution of the central nervous system (CNS) are not well understood. The physiological nature of primitive neurons has not been elucidated, and whether the CNSs of extant bilaterians originated with an array of nerve nets or with a primordial neuronal aggregation is unknown. The nervous systems of cnidarians, the closest sister branch to bilaterians, manifest similarities to bilaterian nervous systems, including developmental mechanisms and cellular features. For example, the cnidarian neurons are electrically excitable, communicating with other neurons or muscles via chemical synapses, and forming diffuse neural networks with significant condensations along the main body axis. Recent genomic and gene expression data from cnidarians and other basal meta-zoans have provided hints to reconstruct the evolutionary history of neurons and the CNS. Genes involved in neuronal physiological functions are conserved among bilaterians, cnidarians, and even sponges. The latter possess sensory cells, but not neurons, providing insights into the origin of neurons. Accumulating evidence shows that cnidarians develop a neural condensation, a " semi-centralized nervous system (semiCNS), " composed of multiple neuronal cell types. Although the development and function of cnidarian nervous systems, especially the semiCNS, remain largely unexplored, numerous molecular signatures shared by cnidarians and bilaterians help us to understand early processes of neural centralization. The anatomically and functionally organized network of a nervous system serves the operational center for animal behaviors. Regionalized condensations of neurons, including the brain of bilaterians, have essential roles for cognitive functions in which neurons process information about ambient stimuli and sometimes store it as individual experiences. At a very early stage of animal evolution, neurons may have originated as unspecialized cells with sensory, neurosecretory, and contractile functions. These ancestral, multifunctional cells became segregated into distinct cell types with either specific sensory, neuronal, or contractile function (Mackie 1970). Neurons formed extended cellular processes, or neurites, connecting to a specific neighboring cells via synapses. This " neural " system seems to have evolved for a rapid and specific signal transmission from sensory cells to a certain specific cell clusters such as a contractile units of muscles and a ciliomotor systems. In contrast to cell– cell communication mediated by undirected diffusion of signaling chemicals, the directed and restricted mode of synaptic communication between connected neurons allows animals to execute coordinated body movements in response to specific environmental contexts. The origin of the nervous system is one of the most exciting questions in biology. There has long been interest in the use of basal metazoans, animal lineages that diverged early in animal evolution, including poriferans, placozoans, ctenophores, and cnidarians (Fig. 3.1)—to understand the early evolutionary processes of animal-specific traits such as the nervous system. In recent years, thanks to sequencing of the basal metazoan genomes, evolutionary biologists have made spectacular advances in unveiling primitive neuronal components. Recent findings in the basal metazoans have also raised several important questions, including whether a nervous system arose only once, or multiple times, and whether neural condensations in bilaterian and cnidarian branches reflect a homologous ancestral nature or a paraphyletic neural characteristics. Answers to these questions are pivotal in reconstructing the molecular and cellular features of the nervous systems that existed in ancestral metazoans. In this chapter, I first provide an overview of genetic repertoires of " neural " components found in basal metazoan genomes and anticipate the genetic and cellular natures of primordial neurons. I then focus on molecular and anatomical features and on physiological functions of the nervous systems in extant cnidarians. Finally, I discuss the nature of primordial neural assemblies that may have been present before divergence of the Cnidaria and Bilateria.