Cuticle differentiation in the embryo of the amphipod crustacean Parhyale hawaiensis

Abstract

The arthropod cuticle is a multilayered extracellular matrix produced by the epidermis during embryogenesis and moulting. Molecularly and histologically, cuticle differentiation has been extensively investigated in the embryo of the insect Drosophila melanogaster. To learn about the evolution of cuticle differentiation, we have studied the histology of cuticle differentiation during embryogenesis of the amphipod crustacean Parhyale hawaiensis, which had a common ancestor with Drosophila about 510 million years ago. The establishment of the layers of the Parhyale juvenile cuticle is largely governed by mechanisms observed in Drosophila, e.g. as in Drosophila, the synthesis and arrangement of chitin in the inner procuticle are separate processes. A major difference between the cuticle of Parhyale and Drosophila concerns the restructuring of the Parhyale dorsal epicuticle after deposition. In contrast to the uniform cuticle of the Drosophila larva, the Parhyale cuticle is subdivided into two regions, the ventral and the dorsal cuticles. Remarkably, the boundary between the ventral and dorsal cuticles is sharp suggesting active extracellular regionalisation. The present analysis of Parhyale cuticle differentiation should allow the characterisation of the cuticle-producing and -organising factors of Parhyale (by comparison with the branchiopod crustacean Daphnia pulex) in order to contribute to the elucidation of fundamental questions relevant to extracellular matrix organisation and differentiation.

Recent advances in understanding mechanisms of insect cuticle differentiation

“…Crustaceans themselves as the first Arthropods arose during the Cambrian explosion around 550 million years ago. Consistent with the close relationship between insects and crustaceans in particular chitin organization is identical in both taxa (Bouligand, 1965;Havemann et al, 2008;Moussian et al, 2006a;Neville and Luke, 1969b). How is chitin organized in sister groups of Arthropods?…”

“…While a discussion of this issue is beyond the scope of this review, I would like to hypothesize that the tracheal luminal chitin is an evolutionary relict from embryonic cuticles that are moulted within the egg case and that are still present in many holo-and hemimetabolous insects and crustaceans (Havemann et al, 2008;Konopova and Zrzavy, 2005;Lagueux et al, 1979;Truman and Riddiford, 1999). The analysis of tracheal morphogenesis in embryos of these insects would help to test this hypothesis.…”

Review of the reproductive biology of amphipods and their endocrine regulation: Identification of mechanistic pathways for reproductive toxicants

“…Moreover, pore canals, which have been proposed to be mineralized or to be routes for mineralization, are present only in the dorsal cuticle. The ventral cuticle resembles the cuticle described for other crustaceans, including copepods, branchiopods, and decapods, whereas the dorsal cuticle seems to be a specific trait of amphipods and isopods [34].…”

“…The outermost lipid and protein-containing envelope is involved in the control of water balance. The middle epicuticle, which is composed of a protein-catecholamine network, and the inner protein-chitin matrix, called the ''procuticle,'' together constitute the stiff, but elastic, exoskeleton [34]. The cuticle of P. hawaiensis is produced by the epidermis during embryogenesis and is renewed during molting.…”

The embryonic development of the malacostracan crustacean Porcellio scaber (Isopoda, Oniscidea)

“…Due to the cuticle formation beginning with stage 18, it was impossible to look at the detailed formation of the pleotelson. Such a formation of a late embryonic or juvenile cuticle is already known for isopods but also for other crustaceans (Powell and Halcrow 1985;Ungerer and Wolff 2005;Havemann et al 2008).…”