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’.

Highlights

  • Reflecting on the benefits that came along with the evolution of the nervous system, a straightforward answer is that it boosted cognition—not the least in ourselves

  • Rather than on isolated vertical circuits, these authors focused on the evolutionary emergence of elementary nerve nets that interconnected receptor cells and/or effector cells horizontally across entire tissues; and addressed the advantages this brought to the functioning of the animal body as a whole

  • Given the remarkable heterogeneity of neuronal cell types— what do the single-cell datasets reveal about the relatedness of these neurons to other, non-neuronal types? Can we identify the neuronal sister cell types? And, what is more, can we identify neuron types that are more closely related to nonneuronal types than they are to other neurons? Such cases would be especially relevant to test the hypothesis of independent neuronal origins—and seem to exist

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Summary

Introduction

Reflecting on the benefits that came along with the evolution of the nervous system, a straightforward answer is that it boosted cognition—not the least in ourselves. The cellular perspective—i.e. the origin of the first neuron—was developed as early as the late nineteenth century by Kleinenberg [4] and the Hertwigs [5], and later refined by Parker [6] These authors derived the first neurons from isolated cells that started to relay to each other and formed elementary circuits, mediating vertical information flow from receptor to effector cells. Rather than on isolated vertical circuits, these authors focused on the evolutionary emergence of elementary nerve nets that interconnected receptor cells and/or effector cells horizontally across entire tissues; and addressed the advantages this brought to the functioning of the animal body as a whole Such early nerve nets would have facilitated coordination and integration of primordial behaviours. This suggests that the non-neural-toneural transition may have occurred more than once, in different tissues and, possibly, distinct evolutionary lineages

Elementary circuits: simple sensory-effector reflex arcs
Conclusion
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