Early axonogenesis in the embryo of a primitive insect, the silverfish Ctenolepisma longicaudata

Abstract

The pattern of axon growth from the population of neurons that pioneers the major axon pathways in the central nervous system is highly conserved in winged insects. This study sought to determine whether the same pattern of axon growth is shared by an apterygotic insect, the silverfish. We have found that homologues to at least nine early differentiating winged insect neurons are present in the silverfish. The axon trajectories and the sequence of axon outgrowth from these neurons are very similar in silverfish and winged insects, suggesting that the pterygotic and apterygotic insects share a common developmental Bauplan for the construction of the central nervous system. Some of these neurons do show differences in several aspects of axon growth, including the relative timing of axonogenesis, the polarity of axon growth and the pattern of axon fasciculation. In addition, a major, early-appearing fascicle in the posterior commissure of the silverfish is pioneered by a neuron which does not appear to have an equivalent in the winged insects. These differences are similar in character to, albeit more pronounced than, differences previously reported between two winged insects, the fruitfly Drosophila and the grasshopper. Some of the features of early central axon growth, that set the silverfish embryo apart from the winged insects, are shared by crustacean embryos, providing support for the claim that insects and crustaceans share a common developmental Bauplan for the construction of central axonal pathways.

Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata : comparison with those seen in flying insects

“…At 27°C the time from oviposition to hatching was about 29 days. For our population, the timing of particular developmental events differed slightly from that reported by Whitington et al (1996).…”

“…Not only were the neuroblasts similar in number and position, but positionally homologous stem cells generated early progeny that showed similar patterns of axonal outgrowth as they pioneered the tracts, commissures, and peripheral nerves. Indeed, Whitington and colleagues (Whitington 1995(Whitington ,1996Whitington et al 1996) report the following set of early neurons as common to Ctenolepisma, Schistocerca and Drosophila. : aCC, pCC, U, RP1, RP2, MP1, vMP2, dMP2, MP4, H, H sib, with cells morphologically similar to those shown in bold also present in crustaceans such as woodlouse and crayfish.…”

Early embryonic development of the central nervous system in the Australian crayfish and the Marbled crayfish (Marmorkrebs)

“…In addition to the arrangement of the median fibre tract, the thoracic ganglia of crayfish and insect embryos share many more architectural features such as the longitudinal fibre tracts (connectives), the segmental and inter-segmental nerves, and the anterior and posterior commissures. It is interesting to note that the posterior commissure of grasshopper thoracic ganglia ) and the anterior and posterior commissures of silverfish embryos (Whitington et al 1996) are composed of two fascicles. Unfortunately, our methods did not allow us to resolve if in crayfish embryos, the commissures are also composed of twin fascicles but this question should be examined in more detail.…”

Larva-adult relationships in an ancestral dipteran: A re-examination of sensillar pathways across the antenna and leg anlagen of Chaoborus crystallinus (DeGeer, 1776; Chaoboridae)

“…Apart from this, the fibres containing neurosecretory vesicles seen in Chaoborus indicate that there is long term regulation of disc development via centrifugal fibres from the CNS (see also Lane et al 1975). The way axonal pathways are formed in the CNS is highly conservative among insects, Pterygota (Goodman and Doe 1993) as well as Apterygota (Whitington et al 1996). As indicated here, the organization of sensory pioneers in insect limbs seems to be evolutionarily conserved between Drosophila and more distantly related insects as well.…”