Neural anatomy of echinoid early juveniles and comparison of nervous system organization in echinoderms

Abstract

The echinoderms are a phylum of marine deuterostomes characterized by the pentaradial (five fold) symmetry of their adult bodies. Due to this unusual body plan, adult echinoderms have long been excluded from comparative analyses aimed at understanding the origin and evolution of deuterostome nervous systems. Here, we investigated the neural anatomy of early juveniles of representatives of three of the five echinoderm classes: the echinoid Paracentrotus lividus, the asteroid Patiria miniata, and the holothuroid Parastichopus parvimensis. Using whole mount immunohistochemistry and confocal microscopy, we found that the nervous system of echinoid early juveniles is composed of three main structures: a basiepidermal nerve plexus, five radial nerve cords connected by a circumoral nerve ring, and peripheral nerves innervating the appendages. Our whole mount preparations further allowed us to obtain thorough descriptions of these structures and of several innervation patterns, in particular at the level of the appendages. Detailed comparisons of the echinoid juvenile nervous system with those of asteroid and holothuroid juveniles moreover supported a general conservation of the main neural structures in all three species, including at the level of the appendages. Our results support the previously proposed hypotheses for the existence of two neural units in echinoderms: one consisting of the basiepidermal nerve plexus to process sensory stimuli locally and one composed of the radial nerve cords and the peripheral nerves constituting a centralized control system. This study provides the basis for more in‐depth comparisons of the echinoderm adult nervous system with those of other animals, in particular hemichordates and chordates, to address the long‐standing controversies about deuterostome nervous system evolution.

The Structure and Function of Gut Microbiomes of Two Species of Sea Urchins, Mesocentrotus nudus and Strongylocentrotus intermedius, in Japan

“…Sea urchin has been used for over a hundred years as a model organism in developmental biology research (Wilson, 1895). Knowledge of sea urchins in the field of biology has expanded to include (1) the effects of toxic substances on their immune system, reproduction, and development (Nobre et al, 2015;Brown et al, 2020;Pikula et al, 2020;Rendell-Bhatti et al, 2021), (2) the gene expression involved in sea urchin fertilization and development stages (Li et al, 2020;Wessel et al, 2021;Cui et al, 2022), (3) the nervous system (Wood et al, 2018;Martín-Durán and Hejnol, 2021;Formery et al, 2021), and (4) sea urchin genomes (Sodergren et al, 2006;Kudtarkar and Cameron, 2017;Kinjo et al, 2018;Warner et al, 2021). Sea urchins have also been studied in various aspects related to the impact of current changing environments, such as ocean acidification and global warming to their development and growth (Dworjanyn and Byrne, 2018;García et al, 2018;Zhao et al, 2018;Houlihan et al, 2020).…”

An easy and rapid staining method for confocal microscopic observation and reconstruction of three‐dimensional images of echinoderm larvae and juveniles

“…(2007) and Formery et al. (2020) for the decalcification procedure. Note: This dehydration step may act as “post‐fixation”. In the original protocol (Amemiya et al., 2019), this step was designed for long‐term sample storage.…”

Nervous System Development and Neuropeptides Characterization in Embryo and Larva: Insights from a Non-Chordate Deuterostome, the Sea Cucumber Apostichopus japonicus

“…Nerve structures, such as neurons located in the apical organ and tracts of axons associated with the ciliary bands were identified during the larval development stage in echinoderms, which matches reports for hemichordate larvae [ 12 , 15 , 16 ]. In recent years, the development of genomic resources and molecular methods have allowed great progress for understanding the mechanisms of neurogenesis in the larvae of many echinoderm species, including the echinoids Strongylocentrotus purpuratus , Paracentrotus lividus , the asteroids Patiria miniata , Asterias rubens , the ophiuroids Amphipholis kochii , the crinoids Antedon mediterranea , Metacrinus rotundus , Anneissia japonica , and also the holothuroids Apostichopus californicus , Apostichopus parvimensis and Apostichopus japonicus [ 2 , 13 , 17 , 18 , 19 , 20 , 21 , 22 ]. These studies all indicated that the larval nervous system shows unexpected diversity in cell and fiber types and their distribution in both central and peripheral nervous components [ 2 , 13 , 17 , 18 , 19 , 20 , 21 , 22 ].…”

“…In recent years, the development of genomic resources and molecular methods have allowed great progress for understanding the mechanisms of neurogenesis in the larvae of many echinoderm species, including the echinoids Strongylocentrotus purpuratus , Paracentrotus lividus , the asteroids Patiria miniata , Asterias rubens , the ophiuroids Amphipholis kochii , the crinoids Antedon mediterranea , Metacrinus rotundus , Anneissia japonica , and also the holothuroids Apostichopus californicus , Apostichopus parvimensis and Apostichopus japonicus [ 2 , 13 , 17 , 18 , 19 , 20 , 21 , 22 ]. These studies all indicated that the larval nervous system shows unexpected diversity in cell and fiber types and their distribution in both central and peripheral nervous components [ 2 , 13 , 17 , 18 , 19 , 20 , 21 , 22 ]. Among echinoderms, the planktotrophic holothuroid sea cucumbers retain both the ancestral body plan and the ancestral nervous system developmental pattern of echinoderms: a lack of neural precursor migration in the embryo and a feeding initiation stage-auricularia followed by a doliolaria stage [ 11 , 23 ].…”

“…Apostichopus japonicus , a classical planktotrophic sea cucumber, has multiple larval strategies and its life cycle can be divided into eight major stages: fertilization (0 hpf (hours post fertilization)), blastula (14 hpf), gastrula (24 hpf), auricularia (48 hpf), doliolaria (11 dpf (days post fertilization)), pentactula (12 dpf), juvenile (16 dpf), and adult [ 24 ]. Although some advances have been made to elucidate certain developmental stages of the holothuroids’ nervous system [ 2 , 21 , 25 ], a comprehensive study of the nervous system from the blastula to pentactula stages has still not been conducted.…”