Evolution of glial wrapping: A new hypothesis

Abstract

Animals are able to move and react in numerous ways to external stimuli. Thus, environmental stimuli need to be detected, information must be processed and finally an output decision must be transmitted to the musculature to get the animal moving. All these processes depend on the nervous system which comprises an intricate neuronal network and many glial cells. In the last decades, a neurono-centric view on nervous system function channeled most of the scientific interest toward the analysis of neurons and neuronal functions. Neurons appeared early in animal evolution and the main principles of neuronal function from synaptic transmission to propagation of action potentials are conserved during evolution. In contrast, not much is known on the evolution of glial cells that were initially considered merely as static support cells. Although it is now accepted that glial cells have an equally important contribution as their neuronal counterpart to nervous system function, their evolutionary origin is unknown. Did glial cells appear several times during evolution? What were the first roles glial cells had to fulfil in the nervous system? What triggered the formation of the amazing diversity of glial morphologies and functions? Is there a possible mechanism that might explain the appearance of complex structures such as myelin in vertebrates? Here, we postulate a common evolutionary origin of glia and depict a number of selective forces that might have paved the way from a simple supporting cell to a wrapping and myelin forming glial cell. K E Y W O R D S evolution, glia, myelinThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Wrapping glia regulates neuronal signaling speed and precision in the peripheral nervous system of Drosophila

“…This separation then results in a reduction of ephaptic coupling and thus electric noise during neuronal signal transmission. This might represent a further evolutionary advantage towards the development of myelin 33 .…”

“…Indeed, swimming speed in copepods does not correlate with myelination 32 . This suggests that wrapping glial cells perform additional tasks than just the acceleration of axon potential propagation speed 33 .…”

Myelin lipids as nervous system energy reserves

“…Oligodendrocytes are glycolytic cells that can provide myelinated axons with lactate or pyruvate for the generation of ATP 5,6,10 . Surprisingly, Drosophila revealed that the metabolic support of axons by associated glia preceded the evolution of myelin in vertebrates 11,12 . In non-myelinating species, notably in Drosophila larvae 13,14 and in lamprey 15 , the axon-associated glial cells that lack myelin accumulate lipid droplets, which are well-known energy reserves 16,17 .…”

Neuron–glia interaction in the Drosophila nervous system

“…Interestingly, compacted myelin is not found in invertebrates but similar morphological specializations have been identified in several invertebrate species such as copepods, earthworms, or shrimps (Davis, Weatherby, Hartline, & Lenz, 1999;Günther, 1976;Roots & Lane, 1983;Xu & Terakawa, 1999). Therefore, it appears possible that the evolutionary origin of myelin formation might have to be placed before the split of invertebrates and vertebrates (see Rey, Zalc, & Klämbt, 2020 for further information, this issue). This is also supported by the molecular mechanisms that regulate simple wrapping in the segmental nerves of the Drosophila PNS.…”