A Key Innovation in Animal Evolution, the Emergence of Neurogenesis: Cellular and Molecular Cues from Cnidarian Nervous Systems

The emergence of neurogenesis led to the acquisition of an efficient neuromuscular transmission in eumetazoans, as shown by cnidarians that use evolutionarily-conserved neurophysiological principles to crumple, feed, swim. However, the cnidarian neuroanatomies are quite diverse and reconstructing the urcnidarian nervous system is not an easy task. Three types of characters shared by anthozoans and medusozoans appear plesiomorphic: 1) three cell types that all cnidarians differentiate, neurosensory cells, ganglionic neurons and nematocytes (cnidocytes) that combine mechano-chemosensation and venom secretion; 2) a chemical conduction through nerve nets and nerve rings, those being considered as annular central nervous systems; 3) a larval apical sensory organ that initiates metamorphosis. Other characters receive a disputed origin: 1) the neural stem cell(s), multipotent interstitial stem cell in hydrozoans, not identified in other classes; 2) the electrical conduction through neurons and epithelial cells present only in hydrozoans; 3) the embryonic origin of the nervous system; 4) the medusa sensory organs, ocelli or lens-eyes for light, statocysts for pressure, lacking in anthozoans. Nevertheless numerous gene families that regulate bilaterian neurogenesis are expressed during cnidarian neurogenesis, e.g. cnidarian eyes express Pax, Six and opsin, supporting a common origin for vision. However data establishing a clear picture of the cnidarian neurogenic circuitry are currently missing. Finally many “neurogenic” gene families likely arose and evolved in the absence of neurogenesis, as exemplified by Porifera that express them but lack synaptic transmission. Therefore some eumetazoan-specific families, missing in Porifera as ParaHox/Hox-like and Otx-like genes, might have contributed to the emergence of neurogenesis