Ophiuroid phylotranscriptomics enables discovery of novel echinoderm representatives of bilaterian neuropeptide families and reconstruction of neuropeptide precursor evolution over ~270 million years

Background Neuropeptides are a diverse class of intercellular signaling molecules that mediate neuronal regulation of many physiological and behavioural processes, including feeding, reproduction and locomotion. Recent advances in genome/transcriptome sequencing are enabling identification of neuropeptide precursor proteins in species from a growing variety of animal taxa, providing new insights into the evolution of neuropeptide signaling. Here we report a phylo-transcriptomic analysis of neuropeptide precursors in over fifty species of brittle stars (Class Ophiuroidea; Phylum Echinodermata).

Results Detailed analysis of transcriptome sequence data from three brittle star species, Ophionotus victoriae, Amphiura filiformis and Ophiopsila aranea, enabled the first comprehensive identification of neuropeptide precursors in ophiuroids. Representatives of over thirty bilaterian neuropeptide precursor families were identified, some of which occur as paralogs (e.g. thyrotropin-releasing hormone, corticotropin-releasing hormone, cholecystokinin, somatostatin and pedal peptide). Furthermore, homologs of endothelin/CCHamide, eclosion hormone, neuropeptide-F/Y and nucleobinin/nesfatin were discovered here in a deuterostome/echinoderm for the first time. The majority of ophiuroid neuropeptide precursors contain a single copy of a neuropeptide, but several precursors comprise multiple copies of identical or non-identical, but structurally-related, neuropeptides. Here we performed an unprecedented investigation of the evolution of neuropeptide copy-number over a period of ~270 million years by analysing sequence data from over fifty ophiuroid species, with reference to a robust phylogeny. Interestingly, the number of neuropeptide copies in the majority of precursors was constant across all the species examined, but examples of clade-specific losses/gains of neuropeptides were also observed.

Conclusions We report here the most comprehensive analysis to date of neuropeptide precursors in the phylum Echinodermata, with novel representatives of several bilaterian neuropeptide families discovered for the first time in echinoderms. Furthermore, analysis of precursor proteins comprising multiple copies of identical or related neuropeptides across ~270 million years of ophiuroid evolution indicates that the composition of neuropeptide “cocktails” is functionally important, but with plasticity over long evolutionary time scales.