Elementary nervous systems

Abstract

The evolutionary origin of the nervous system has been a matter of long-standing debate. This is due to the different perspectives taken. Earlier studies addressed nervous system origins at the cellular level. They focused on the selective advantage of the first neuron in its local context, and considered vertical sensory-motor reflex arcs the first nervous system. Later studies emphasized the value of the nervous system at the tissue level. Rather than acting locally, early neurons were seen as part of an elementary nerve net that enabled the horizontal coordination of tissue movements. Opinions have also differed on the nature of effector cells. While most authors have favoured contractile systems, others see the key output of the incipient nervous system in the coordination of motile cilia, or the secretion of antimicrobial peptides. I will discuss these divergent views and explore how they can be validated by molecular and single-cell data. From this survey, possible consensus emerges: (i) the first manifestation of the nervous system likely was a nerve net, whereas specialized local circuits evolved later; (ii) different nerve nets may have evolved for the coordination of contractile or cilia-driven movements; (iii) all evolving nerve nets facilitated new forms of animal behaviour with increasing body size. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.

Single-cell RNA sequencing of the Strongylocentrotus purpuratus larva reveals the blueprint of major cell types and nervous system of a non-chordate deuterostome

“…In fact, based on these findings a close evolutionary link between endoderm and ectoderm has been postulated ( Steinmetz et al, 2017 ). Finally, motor neurons in the vertebrate ventral neural tube and pancreatic islet cells share a specific combination of transcription factors including pax6, nkx6 , and hb9 (reviewed in Arendt, 2021 ). Overall, this second possibility is also in line with the hypothesis that at least subsets of neuron types in animal nervous systems may have originated from a mucociliary sole that initially harbored a neurosecretory network of cells with digestive and communicative functions ( Arendt et al, 2015 ; Arendt, 2021 ).…”

Uncovering cognitive similarities and differences, conservation and innovation

“…Starting more than 150 years ago, this led to the notion that the first manifestation of the nervous system was a simple vertical sensory-effector arc-most prominently in Parker's 'elementary nervous system' [39]. In a comprehensive history of thought in this domain, Arendt [40] surveys the long path from these initial ideas to modern hypotheses on nervous system origins, culminating in the consensus that the early nervous system was indeed an elementary nerve net. These nets acted as endogenous pacemakers and integrated sensory input for the coordinated control of entire downstream effector tissues-which may have been contractile or bearing motile cilia.…”

Multiple Origins of Neurons From Secretory Cells

“…The diversity of low molecular weight and peptide transmitters in all animals triggered several attempts to incorporate transmitter signaling in neuronal evolution models. Several recent publications provided different historical outlines and perspectives of this endeavor (Moroz, 2009 , 2014 ; Moroz and Kohn, 2015 , 2016 ; Arendt, 2021 ; Jekely, 2021 ; Moroz et al, 2021 ), which are not yet integrated into a comprehensive and unbiased review of the subject.…”

“…However, in this scenario, the evolutionary predecessors of neurons and muscles were myoepithelial cells. The emerging single-cell sequencing data in Hydra (Siebert et al, 2019 ) showed that selected muscle and neuronal cells in cnidaria might share some transcriptional factors summarized in the recent review (Arendt, 2021 ). Of note, striated muscle cells also evolved at least two-three times in evolution (Steinmetz et al, 2012 ).…”