Nervous system characterization during the development of a basal echinoderm, the feather star Antedon mediterranea

Abstract

Neural development of echinoderms has always been difficult to interpret, as larval neurons degenerate at metamorphosis and a tripartite nervous system differentiates in the adult. Despite their key phylogenetic position as basal echinoderms, crinoids have been scarcely studied in developmental research. However, since they are the only extant echinoderms retaining the ancestral body plan of the group, crinoids are extremely valuable models to clarify neural evolution in deuterostomes. Antedon mediterranea is a feather star, endemic to the Mediterranean Sea. Its development includes a swimming lecithotrophic larva, the doliolaria, with basiepithelial nerve plexus, and a sessile filter‐feeding juvenile, the pentacrinoid, whose nervous system has never been described in detail. Thus, we characterized the nervous system of both these developmental stages by means of immunohistochemistry and, for the first time, in situ hybridization techniques. The results confirmed previous descriptions of doliolaria morphology and revealed that the larval apical organ contains two bilateral clusters of serotonergic cells while GABAergic neurons are localized under the adhesive pit. This suggested that different larval activities (e.g., attachment and metamorphosis) are under the control of different neural populations. In pentacrinoids, the analysis showed the presence of a cholinergic entoneural system while the ectoneural plexus appeared more composite, displaying different neural populations. The expression of three neural‐related microRNAs was described for the first time, suggesting that these are evolutionarily conserved also in basal echinoderms. Overall, our results set the stage for future investigations that will reveal new information on echinoderm evo‐devo neurobiology.

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

“…Serotonergic neurons are the first neurons to differentiate in most echinoderm and hemichordate species and are thought to be primary sensory neurons with short apical dendritic poles and basal axonal projections [ 12 , 16 ]. In the late gastrula stage, we observed serotonin-positive immunoreactions in the anterior apical region, that matches the discovery in echinoderms, hemichordates, and protostomes with swimming larvae [ 2 , 12 , 13 , 18 , 79 , 80 , 81 ]. Interestingly, serotonergic immunoreactions were also identified in the ciliary band of A. japonicus embryos and larvae, supporting the potential role of serotonin in the modulation of ciliary beating and metamorphosis.…”

“…It was clearer in the larvae stained by an acetylated α-tubulin antibody, which is widely used as a pan-neuronal marker labeling neurites and cilia [ 69 , 70 , 84 ]. Acetylated α-tubulin was found in the ciliary band or ring at all developmental stages in A. japonicus and regularly spaced within the ciliary rings in doliolaria and early pentactula larvae, which is consistent with the dipleurula-type larvae of sea urchin, starfish, brittle star and feather star echinoderms, and evolutionarily closely related cephalochordates and hemichordates [ 13 , 18 , 21 , 69 , 70 , 85 ]. Our observation supports the possible principal role of the ciliary band in locomotion and feeding, which is possibly controlled by the nervous system in echinoderm larvae [ 16 , 86 , 87 ].…”

“…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 ].…”

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

“…In comparison, the adult nervous system of echinoderms has received much less attention. Most studies on echinoderm adult nervous systems have so far been focused on the histological characterization of their anatomy and ultrastructure (Hyman, 1955; Mashanov, Zueva, Rubilar, Epherra, & Garcia‐Arraras, 2016; Smith, 1965), with little characterization of the molecular details of their development or anatomy, compared to larvae (e.g., Adachi et al, 2018; Mashanov, Zueva, & Garcia‐Arraras, 2015; Mercurio, Gattoni, Messinetti, Sugni, & Pennati, 2019; Sumner‐Rooney, Rahman, Sigwart, & Ullrich‐Lüter, 2018; Tinoco et al, 2018). Furthermore, an integrated and comprehensive description of the neural organization of echinoderm adult nervous systems is still lacking, and it is still unclear to what extent this detailed organization is conserved across the different echinoderm classes.…”