Abstract

Neuropeptides are among the structurally most diverse signaling molecules and participate in intercellular information transfer from neurotransmission to intrinsic or extrinsic neuromodulation. Many of the peptidergic systems have a very ancient origin that can be traced back to the early evolution of the Metazoa. In recent years, new insights into the evolution of these peptidergic systems resulted from the increasing availability of genome and transcriptome data which facilitated the investigation of the complete neuropeptide precursor sequences. Here we used a comprehensive transcriptome dataset of about 200 species from the 1KITE initiative to study the evolution of single-copy neuropeptide precursors in Polyneoptera. This group comprises well-known orders such as cockroaches, termites, locusts, and stick insects. Due to their phylogenetic position within the insects and the large number of old lineages, these insects are ideal candidates for studying the evolution of insect neuropeptides and their precursors. Our analyses include the orthologs of 21 single-copy neuropeptide precursors, namely ACP, allatotropin, AST-CC, AST-CCC, CCAP, CCHamide-1 and 2, CNMamide, corazonin, CRF-DH, CT-DH, elevenin, HanSolin, NPF-1 and 2, MS, proctolin, RFLamide, SIFamide, sNPF, and trissin. Based on the sequences obtained, the degree of sequence conservation between and within the different polyneopteran lineages is discussed. Furthermore, the data are used to postulate the individual neuropeptide sequences that were present at the time of the insect emergence more than 400 million years ago. The data confirm that the extent of sequence conservation across Polyneoptera is remarkably different between the different neuropeptides. Furthermore, the average evolutionary distance for the single-copy neuropeptides differs significantly between the polyneopteran orders. Nonetheless, the single-copy neuropeptide precursors of the Polyneoptera show a relatively high degree of sequence conservation. Basic features of these precursors in this very heterogeneous insect group are explained here in detail for the first time.

Highlights

  • Neuropeptides are among the structurally most diverse signaling molecules in multi-cellular animal organisms

  • The BLAST searches in the Polyneoptera transcriptome assemblies of the 1KITE initiative were performed with singlecopy neuropeptide precursor sequences of C. morosus [2], L. migratoria [1], and Blattodea [3]

  • The yield of neuropeptide precursors is different for the different precursors; for example, much fewer CCHamide-1 precursors could be identified across the different lineages than precursors for other neuropeptides such as proctolin and neuropeptide F-1 (NPF-1)

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Summary

Introduction

Neuropeptides are among the structurally most diverse signaling molecules in multi-cellular animal organisms. As such, they participate in intercellular information transfer from neurotransmission to intrinsic or extrinsic neuromodulation and regulate physiological processes including growth, reproduction, development, and behavior. Evolution of Neuropeptide Precursors neuropeptide genes can be expected coding for single or multiple copies of neuropeptides [1, 2]. The sequences of single-copy neuropeptides, which are the focus of our study, are on average better conserved than those of multiple-copy peptides because amino acid (AA) substitutions in the single ligand of a particular neuropeptide receptor are potentially more likely to lead to a general loss of function than substitutions involving only one of several related neuropeptides produced from the same precursor. Elphick et al [4] have described as much as 30 neuropeptide signaling systems with orthologs in protostomes and deuterostomes

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