Ancient origins of arthropod moulting pathway components
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 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.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have also been provide. The molecular databases analysed in this study are publicly available and novel annotated sequences are included in the Supplementary Data. The list of investigated species and their respective links to a direct download are presented in the Supplementary File 1 (Table S1). The 3D proneuropeptide/ prohormone maps (showed in the Figures 1 and 3), as well as all the multiple sequence alignments, and phylogenetic trees generated in this study are available in the Supplementary data enclosed in the original submission. The 3D maps in .rtf format can be visualised and inspected with the software clans (ftp://ftp.tuebingen.mpg.de/pub/protevo/CLANS/). The multiple sequence alignments used in the phylogenetic inferences can be graphically visualised using aliview (http://www.ormbunkar.se/aliview/#DOWNLOAD). The phylogenetic tree files can be viewed using an appropriate phylogetic tree viewer such as Figtree (http://tree.bio.ed.ac.uk/software/figtree/).
Article and author information
Author details
Funding
Austrian Science Fund (P29455-B29)
- Andreas Wanninger
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (6090/13-3)
- André Luiz de Oliveira
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India
Version history
- Received: February 14, 2019
- Accepted: June 27, 2019
- Accepted Manuscript published: July 3, 2019 (version 1)
- Version of Record published: July 26, 2019 (version 2)
Copyright
© 2019, de Oliveira et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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Extant ecdysozoans (moulting animals) are represented by a great variety of soft-bodied or articulated organisms that may or may not have appendages. However, controversies remain about the vermiform nature (i.e. elongated and tubular) of their ancestral body plan. We describe here Beretella spinosa gen. et sp. nov. a tiny (maximal length 3 mm) ecdysozoan from the lowermost Cambrian, Yanjiahe Formation, South China, characterized by an unusual sack-like appearance, single opening, and spiny ornament. Beretella spinosa gen. et sp. nov has no equivalent among animals, except Saccorhytus coronarius, also from the basal Cambrian. Phylogenetic analyses resolve both fossil species as a sister group (Saccorhytida) to all known Ecdysozoa, thus suggesting that ancestral ecdysozoans may have been non-vermiform animals. Saccorhytids are likely to represent an early off-shot along the stem-line Ecdysozoa. Although it became extinct during the Cambrian, this animal lineage provides precious insight into the early evolution of Ecdysozoa and the nature of the earliest representatives of the group.