Abstract

The origin and extreme diversification of the animal nervous system is a central question in biology. While most of the attention has traditionally been paid to those lineages with highly elaborated nervous systems (e.g. arthropods, vertebrates, annelids), only the study of the vast animal diversity can deliver a comprehensive view of the evolutionary history of this organ system. In this regard, the phylogenetic position and apparently conservative molecular, morphological and embryological features of priapulid worms (Priapulida) place this animal lineage as a key to understanding the evolution of the Ecdysozoa (i.e. arthropods and nematodes). In this study, we characterize the nervous system of the hatching larva and first lorica larva of the priapulid worm Priapulus caudatus by immunolabelling against acetylated and tyrosinated tubulin, pCaMKII, serotonin and FMRFamide. Our results show that a circumoral brain and an unpaired ventral nerve with a caudal ganglion characterize the central nervous system of hatching embryos. After the first moult, the larva attains some adult features: a neck ganglion, an introvert plexus, and conspicuous secondary longitudinal neurites. Our study delivers a neuroanatomical framework for future embryological studies in priapulid worms, and helps illuminate the course of nervous system evolution in the Ecdysozoa.

Highlights

  • The animal nervous system is the specialized set of cells, tissues and organs responsible for integrating external and internal stimuli and coordinating adequate responses

  • Our results show that a circumoral brain and an unpaired ventral nerve with a caudal ganglion characterize the central nervous system of hatching embryos

  • The immunoreactivity patterns of five different antibodies commonly used in neuroanatomical analyses demonstrate that priapulid embryos hatch with a nervous system composed of a circumoral brain and an apparently unpaired ventral nerve ending in a caudal ganglion

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Summary

Introduction

The animal nervous system is the specialized set of cells, tissues and organs responsible for integrating external and internal stimuli and coordinating adequate responses. In adults and mature priapulid larvae, the central nervous system (CNS) is intraepidermal and comprises a circumoral brain, an unpaired ventral nerve cord and two main ganglia, the neck ganglion at the joint between the introvert and the trunk and the caudal ganglion at the most posterior region of the body [38,39]. To gain a better knowledge of the early stages of nervous system formation in priapulid worms, we analysed the immunostaining domains of five antibodies commonly used to characterize neural structures in ecdysozoan animals [2,38,42 –51] in hatching larvae and first lorica larvae of the species Priapulus caudatus Lamarck, 1816. (d ) The introvert region of the first lorica larva is rich in neural fibres, with a dense innervation of the scalids from the brain area (black dashed circle; main ventral nerve indicated by green arrowheads and the neck commissures by blue arrowheads).

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