Novel organization and development of copepod myelin. i. ontogeny

Abstract

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.

Escapes in copepods: comparison between myelinate and amyelinate species

“…Copepodites of the myelinate species had the ability to detect the location of the stimulus and react appropriately; this difference was not observed in nauplii. Early developmental stages (nauplii) have less well developed antennular sensory systems (Boxshall and Huys, 1998), they use the antennule for locomotion (Lenz et al, 2015), they are less sensitive to hydromechanical stimuli (Bradley et al, 2013), and the nauplii of myelinate species possess much less myelin (Wilson and Hartline, 2011). Thus, it is not surprising that the differences between myelinate and amyelinate species are not present in nauplii, but become apparent in the copepodite form.…”

“…While calanoid copepods can be divided into two large groups based on their myelin (Davis et al, 1999;Lenz et al, 2000), their physiology, anatomy and behavior are similar. The musculature of the swimming legs and the force output during the escape are similar (Boxshall, 1992;Hartline et al, 1999;Lenz and Hartline, 1999;Lenz et al, 2000), as is the organization of their nervous system, including the innervation of the escape circuitry Lowe, 1935;Park, 1966;Wilson and Hartline, 2011). Both possess highly sensitive antennular mechanoreceptors that are similar in structure (Weatherby and Lenz, 2000;Yen et al, 1992); and both use either antennular sweeps or a backward rotation to redirect their escape swim (Gill, 1986;Gill and Crips, 1985;Lenz et al, 2004;Park, 1966).…”

The “Lillie Transition”: models of the onset of saltatory conduction in myelinating axons

“…Vertebrates that have little if any myelin at birth or hatching myelinate their originally continuously-conducting axons through a significant portion of postnatal existence (e.g. Carpenter and Bergland 1975;Foster et al 1982;Vabnick andShrager 1999, Brösamle andHalpern 2002), and axons in myelinate invertebrates also transition from unmyelinated to myelinated in the course of development (Xu et al 1994;Wilson and Hartline 2011). Its occurrence in evolution is exemplified by the myelinated dorsal giant axons of shrimp, which have unmyelinated presumed homologues in the more basal Malacostraca (Freidländer 1889), and the myelinated Mauthner cells of fish, which are unmyelinated among the lampreys (Rovainen 1967).…”

“…The changeover between unmyelinated and myelinated states has major consequences for the operational characteristics of the nervous system (e.g. changes in feedback loop and delay-line timing, muscle synchrony, etc; Seidl et al 2010;Wilson and Hartline 2011), as well as potential difficulties to be surmounted for a smooth transition. It is not altogether clear how smooth such a transition might be under various assumed conditions, since abrupt changes in electrical properties in an axon (among which conduction mode might be included) can lead to spike failure or reflections (Goldstein and Rall 1974;Calvin and Hartline 1977).…”

The Evolution of Myelin: Theories and Application to Human Disease

“…Intriguingly copepod myelin seems to be neurally, rather than glially derived, developing by sequential laying down of membrane layers on the inside of the axon membrane [47,48]. This explains the continuous structure; one possible application of this discovery is discussed in Section 3.…”