Nerve impulse conduction is greatly increased by myelin, a multilayered membranous sheath surrounding axons. Best known from and most extensively investigated among vertebrates, a few invertebrates, including some superfamilies of copepod, have functionally and structurally similar myelin-like sheaths surrounding their axons. We examined the development of myelin ultrastructure in Bestiolina similis, a paracalanoid copepod. Development occurred in a novel way: initial myelination always appeared first as a partial layer, which in later stages came to encircle an axon completely. This partial myelin first appeared in a single pair of reidentifiable fibers, at the second naupliar stage. Two additional pairs of reidentifiable fibers also became partially myelinated by the third naupliar stage. The number of myelin layers in this trio of axon pairs increased with development, but, at any one stage, each axon had the same number of layers along its entire length. These axons disappeared after the copepodite metamorphosis. After metamorphosis, the fiber that took over as largest in the nerve cord became the most heavily myelinated and was identified as the lateral dorsal giant fiber. The rate of myelination was also characterized in the antennular nerve as a representative of the peripheral nervous system. As axons became larger, they were more likely to be partially, and then completely, myelinated, the latter having a lower ratio of axon core to fiber diameter than the former. Copepod myelin is an instructive example of convergent evolution, with far-reaching consequences for nervous system functioning and the behavior that nervous systems subserve.
Nerve-impulse conduction is greatly speeded by myelin sheaths in vertebrates, oligochaete annelids, penaeid and caridean shrimp, and calanoid copepods. In the first three invertebrate cases, myelin arises from glial cells, as it does in vertebrates. The contribution of the glial cells to the layered structure of the myelin is clear: their nuclei are either embedded in the layers or reside in contiguous cytoplasmic compartments, and their cell membranes are seen to be continuous with those of the myelin layers. However, with calanoids, the association with glial cells presumed necessary to generate the myelin has never been satisfactorily identified. We have conducted a systematic examination of thin sections through different parts of the copepod nervous system to identify the structural organization of copepod myelin and the likely mechanism for its formation. We find that myelination appears to commence by laying down and compacting a cisternal tongue against the inside of the axolemma. This is followed by the successive layering and compaction of additional tongues to create a stack of tongues. The margins of the tongues then expand to encircle the interior of a neurite, meeting and fusing to form complete concentric myelin. No sign of glial involvement could be detected at any stage. Unlike glially derived myelin, the extracellular tracer lanthanum did not penetrate between the myelin layers in copepods, further evidence against a glial source. We believe this to be the first demonstration of a nonglial origin for myelin in any species.
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