Ultrastructure, development, and homology of insect embryonic cuticles

Abstract

Ultrastructure and deposition of the cuticles secreted by embryos representing eight insect orders were examined by transmission and scanning electron microscopy. Embryos of the apterygote silverfish Thermobia domestica deposit two embryonic cuticles. Deposition of the first (EC1) is initiated at the beginning of appendage development when the intercalary segment and the neural groove are clearly visible. This cuticle lacks surface microsculpture and consists of an outer epicuticle and an underlying fibrous layer, thought to represent procuticle. At the time of dorsal closure, deposition of a second embryonic cuticle (EC2) begins; this bears sensilla and functions in the first instar larva. In representative embryos of seven pterygote orders (Ephemeroptera, Odonata, Plecoptera, Neuroptera, Coleoptera, Lepidoptera, and Mecoptera), three cuticles were found to be secreted. The first cuticle in pterygotes is homologous to EC1 of T. domestica, but consists solely of outer epicuticle. EC2, the "prolarval cuticle," bears a characteristic surface microsculpture in embryos of some species and egg-teeth and other hatching devices, and consists of outer and inner epicuticles and a more or less reduced procuticle. EC2 is reduced in the embryos of derived endopterygotes, where a procuticle is lacking and the inner epicuticle is reduced. After hatching, when EC2 is shed, the first instar larva is covered by a third embryonic cuticle (EC3), whose deposition was initiated while the insect was still within the egg. Presence of only two embryonic cuticles in cyclorrhaphous flies is due to the total loss of prolarval cuticle. Investigated exopterygote and endopterygote insects excluding flies thus deposit three embryonic cuticles, and their juveniles (exopterygote "nymphs"; endopterygote "larvae") seem to hatch at equivalent stages of development. Differences between the modes of cuticulogenesis in silverfish and pterygote embryos suggest that the apterygote first larval instar was embryonized and became a fully embryonic prolarva in pterygotes.

From embryo to adult—beyond the conventional periodization of arthropod development

“…Looking for equivalence between stages could thus be meaningless. More subtly, biases may rise in evaluating hypotheses of evolutionary change for developmental traits, which may be (unconsciously) confined to a limited set of alternatives (e.g., Konopová andZrzavý 2005 vs Truman andRiddiford 1999). Instars are not slots of development that can only fuse, split, and shift forward or backward with respect to other developmental events.…”

“…The exception is cyclorrhaphous flies, with only two embryonic cuticles. In the opinion of Konopová and Zrzavý (2005), however, peculiarities of cuticulogenesis would suggest that in the transition from apterygote to pterygote (compare, e.g., the silverfish with a mayfly or a dragonfly), the first postembryonic (larval) instar of apterygotes has become embryonized in pterygotes. That is, the link between hatching and molting is not fixed, even within the insect lineage.…”

“…For example, the way we interpret the stages immediately before 1and after hatching has a strong relevance to our views on the possible origin of holometaboly. Konopová and Zrzavý (2005), for example, contend that exopterygotes and endopterygotes hatch at equivalent stages because their embryos all shed three embryonic cuticles. The exception is cyclorrhaphous flies, with only two embryonic cuticles.…”

Development of respiratory structures in embryos and first and second instars of the bark scorpion, Centruroides gracilis (Scorpiones: Buthidae)

“…For insect embryonic cuticles, hypodermal cells with microvilli release electron-dense plaques that form a cuticle layer (Konopová and Zrzavý, 2005). Large protein and polysaccharide molecules (chitin) from hypodermal cells aggregate spontaneously to form the insect exoskeleton (Merzendorfer and Zimoch, 2003;Merzendorfer, 2006).…”

Observations of Embryonic Changes in Middle and Late Stages of the Greater Wax Moth, <i>Galleria mellonella</i> (Lepidoptera: Pyralidae)

“…Dorsal closure in Manducasexta states that is nearly complete when the embryo undergoes the katatrepsis movement [20], while in G. mellonella embryos, the dorsal closure starts during the katatrepsis process.…”