Changes in the neuropeptide complement correlate with nervous system architectures in xenacoelomorphs

Abstract

Neuropeptides are essential neurosecretory signaling molecules common in protostomes and deuterostomes (together Nephrozoa). Not much, however, is known about the neuropeptide complement of the sister group Xenacoelomorpha. This group is comprised of the three clades Xenoturbella, Nemertodermatida, and Acoela, which differ strongly in their nervous system anatomy. In order to reconstruct the ancestral bilaterian neuropeptide complement and gain insights into neuropeptide evolution within Xenacoelomorpha, we analyzed transcriptomes of 13 acoels, nemertodermatids, and Xenoturbella species. Together with motif searches, similarity searches, mass spectrometry and phylogenetic analyses of neuropeptide precursors and neuropeptide receptors, we reconstruct the xenacoelomorph neuropeptide complement. Our comparison of xenacoelomorph GPCRs with cnidarian and nephrozoan neuropeptide receptors shows that the neuropeptide signaling diversified into at least 20 ancestral peptidergic systems in the lineage to Bilateria. We find that Xenoturbella species possess many of the ancestral bilaterian peptidergic systems and only a few clade-specific neuropeptides. Nemertodermatids seem to have nearly the complete complement of ancestral bilaterian systems and several novel neuropeptides. Acoels show an extensive loss of conserved bilaterian systems, but gained the highest number of novel and group-specific neuropeptides. While it is difficult to correlate the emergence of the bilaterian neuropeptide complement with the evolution of centralized nervous systems, we find a correlation between nervous system novelties and the expansion of taxon-specific neuropeptides in Xenacoelomorpha.