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

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