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Ancestral Role of Ecdysis-Related Neuropeptides in Animal Life Cycle Transitions

2020; Elsevier BV; Volume: 31; Issue: 1 Linguagem: Inglês

10.1016/j.cub.2020.10.004

1879-0445

Elisabeth Zieger, Nicolas Robert, Andrew D. Calcino, Andreas Wanninger,

Circadian rhythm and melatonin

Ecdysis or molting evolved ∼535 mya in Ecdysozoa, the most diverse and species-rich animal superphylum.1Wang D. Vannier J. Schumann I. Wang X. Yang X.-G. Komiya T. Uesugi K. Sun J. Han J. Origin of ecdysis: fossil evidence from 535-million-year-old scalidophoran worms.Proc. Biol. Sci. 2019; 286: 20190791PubMed Google Scholar A cascade of ecdysis-related neuropeptides (ERNs) controls the innate behavioral programs required for cuticle shedding in some ecdysozoan lineages (e.g., arthropods)2Ewer J. How the ecdysozoan changed its coat.PLoS Biol. 2005; 3: e349Crossref PubMed Scopus (31) Google Scholar, 3White B.H. Ewer J. Neural and hormonal control of postecdysial behaviors in insects.Annu. Rev. Entomol. 2014; 59: 363-381Crossref PubMed Scopus (42) Google Scholar, 4Nässel D.R. Zandawala M. Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior.Prog. Neurobiol. 2019; 179: 101607Crossref PubMed Scopus (91) Google Scholar, 5Kim D.-H. Han M.-R. Lee G. Lee S.S. Kim Y.-J. Adams M.E. Rescheduling behavioral subunits of a fixed action pattern by genetic manipulation of peptidergic signaling.PLoS Genet. 2015; 11: e1005513Crossref PubMed Scopus (29) Google Scholar, 6Zitnan D. Adams M.E. Neuroendocrine regulation of ecdysis.in: Gilbert L.I. Insect Endocrinology. Elsevier, 2012: 253-309Crossref Scopus (68) Google Scholar, 7Wulff J.P. Capriotti N. Ons S. Orcokinins regulate the expression of neuropeptide precursor genes related to ecdysis in the hemimetabolous insect Rhodnius prolixus.J. Insect Physiol. 2018; 108: 31-39Crossref PubMed Scopus (15) Google Scholar, 8Lee D. Orchard I. Lange A.B. Evidence for a conserved CCAP-signaling pathway controlling ecdysis in a hemimetabolous insect, Rhodnius prolixus.Front. Neurosci. 2013; 7: 207Crossref PubMed Scopus (30) Google Scholar, 9Lenaerts C. Cools D. Verdonck R. Verbakel L. Vanden Broeck J. Marchal E. The ecdysis triggering hormone system is essential for successful moulting of a major hemimetabolous pest insect, Schistocerca gregaria.Sci. Rep. 2017; 7: 46502Crossref PubMed Scopus (29) Google Scholar, 10Webster S.G. Wilcockson D.C. Mrinalini Sharp J.H. Bursicon and neuropeptide cascades during the ecdysis program of the shore crab, Carcinus maenas.Gen. Comp. Endocrinol. 2013; 182: 54-64Crossref PubMed Scopus (34) Google Scholar, 11Oliphant A. Alexander J.L. Swain M.T. Webster S.G. Wilcockson D.C. Transcriptomic analysis of crustacean neuropeptide signaling during the moult cycle in the green shore crab, Carcinus maenas.BMC Genomics. 2018; 19: 711Crossref PubMed Scopus (33) Google Scholar, 12Zhou L. Li S. Wang Z. Li F. Xiang J. An eclosion hormone-like gene participates in the molting process of Palaemonid shrimp Exopalaemon carinicauda.Dev. Genes Evol. 2017; 227: 189-199Crossref PubMed Scopus (14) Google Scholar but is lacking in others (e.g., nematodes).13de Oliveira A.L. Calcino A. Wanninger A. Ancient origins of arthropod moulting pathway components.eLife. 2019; 8: e46113Crossref PubMed Scopus (14) Google Scholar We recently reported on the surprisingly ancient bilaterian origin of key ERNs, such as eclosion hormone (EH), crustacean cardioactive neuropeptide (CCAP), myoinhibitory peptide (MIP), bursicon alpha (Bursα), and bursicon beta (Bursβ).13de Oliveira A.L. Calcino A. Wanninger A. Ancient origins of arthropod moulting pathway components.eLife. 2019; 8: e46113Crossref PubMed Scopus (14) Google Scholar,14De Oliveira A.L. Calcino A. Wanninger A. Extensive conservation of the proneuropeptide and peptide prohormone complement in mollusks.Sci. Rep. 2019; 9: 4846Crossref PubMed Scopus (10) Google Scholar Thus, ERNs far predate the emergence of ecdysis, but the question as to their ancestral functions remains unresolved. Here, we compare the ERN toolkits and temporal expression profiles of six ecdysozoans (tardigrades, crustaceans, and insects), eight lophotrochozoans (planarians, annelids, and mollusks), and five deuterostomes (crinoids, sea urchins, and hemichordates). Our results show that the major, coordinated upregulation of ERNs always coincides with a transition between key life history stages, such as hatching in direct developers and metamorphosis in indirect developers. This implies that ERNs already played an ancestral role in the switch from embryonic or larval ontogeny to juvenile maturation in the last common ancestor of Nephrozoa. Consequently, the transcriptional signature of invertebrate life cycle transitions presented here was already in place in the Precambrian and was only secondarily co-opted into regulating the molting process at the dawn of Ecdysozoa.