Abstract

Ecdysis (moulting) is the defining character of Ecdysoza (arthropods, nematodes and related phyla). Despite superficial similarities, the signalling cascade underlying moulting differs between Panarthropoda and the remaining ecdysozoans. Here, we reconstruct the evolution of major components of the ecdysis pathway. Its key elements evolved much earlier than previously thought and are present in non-moulting lophotrochozoans and deuterostomes. Eclosion hormone (EH) and bursicon originated prior to the cnidarian-bilaterian split, whereas ecdysis-triggering hormone (ETH) and crustacean cardioactive peptide (CCAP) evolved in the bilaterian last common ancestor (LCA). Identification of EH, CCAP and bursicon in Onychophora and EH, ETH and CCAP in Tardigrada suggests that the pathway was present in the panarthropod LCA. Trunk, an ancient extracellular signalling molecule and a well-established paralog of the insect peptide prothoracicotropic hormone (PTTH), is present in the non-bilaterian ctenophore Mnemiopsis leidyi. This constitutes the first case of a ctenophore signalling peptide with homology to a neuropeptide.

Highlights

  • Ecdysis or moulting, which describes the process of shedding the outer integument, the cuticle, is a defining feature of Ecdysozoa (Aguinaldo et al, 1997; Schmidt-Rhaesa et al, 1998; de Rosa et al, 1999; Dunn et al, 2008; Telford et al, 2008)

  • Studies in insects have revealed that the major components of this peptidergic signalling pathway are ecdysis-triggering hormone (ETH), eclosion hormone (EH), crustacean cardioactive peptide (CCAP) and bursicon (Gammie and Truman, 1997a; Gammie and Truman, 1997b; Zitnan et al, 1999; Clark et al, 2004; Kim et al, 2006a; Kim et al, 2006b; Arakane et al, 2008; Lee et al, 2013)

  • prothoracicotropic hormone (PTTH) is a neurohormone with a proposed origin at the base of Arthropoda that is believed to have evolved from the duplication of the ancient and widely distributed bilaterian signalling moleculeencoding gene trunk (Rewitz et al, 2009; Jekely, 2013)

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Summary

Introduction

Ecdysis or moulting, which describes the process of shedding the outer integument, the cuticle, is a defining feature of Ecdysozoa (arthropods, tardigrades, onychophorans, nematodes and related phyla) (Aguinaldo et al, 1997; Schmidt-Rhaesa et al, 1998; de Rosa et al, 1999; Dunn et al, 2008; Telford et al, 2008). Despite superficial similarities of the ‘moulting behaviour’ within Ecdysozoa, the neuroendocrine components underlying this process remain elusive for the majority of the ecdysozoans outside of Arthropoda This includes well-established model organisms such as the nematode Caenorhabditis elegans, for which the gene regulatory network responsible for ecdysis remains to be fully resolved (Frand et al, 2005; reviewed by Page et al, 2014 and Lazeticand Fay, 2017). The decline of the ecdysone titre due to the ecdysone-inactivating enzyme cytochrome P450 protein Cyp18a1 (Guittard et al, 2011; reviewed by Rewitz et al, 2013) triggers the release of ETH that, in turn, causes the release of EH

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