Developmental atlas of the indirect-developing sea urchin Paracentrotus lividus: From fertilization to juvenile stages

Abstract

The sea urchin Paracentrotus lividus has been used as a model system in biology for more than a century. Over the past decades, it has been at the center of a number of studies in cell, developmental, ecological, toxicological, evolutionary, and aquaculture research. Due to this previous work, a significant amount of information is already available on the development of this species. However, this information is fragmented and rather incomplete. Here, we propose a comprehensive developmental atlas for this sea urchin species, describing its ontogeny from fertilization to juvenile stages. Our staging scheme includes three periods divided into 33 stages, plus 15 independent stages focused on the development of the coeloms and the adult rudiment. For each stage, we provide a thorough description based on observations made on live specimens using light microscopy, and when needed on fixed specimens using confocal microscopy. Our descriptions include, for each stage, the main anatomical characteristics related, for instance, to cell division, tissue morphogenesis, and/or organogenesis. Altogether, this work is the first of its kind providing, in a single study, a comprehensive description of the development of P. lividus embryos, larvae, and juveniles, including details on skeletogenesis, ciliogenesis, myogenesis, coelomogenesis, and formation of the adult rudiment as well as on the process of metamorphosis in live specimens. Given the renewed interest for the use of sea urchins in ecotoxicological, developmental, and evolutionary studies as well as in using marine invertebrates as alternative model systems for biomedical investigations, this study will greatly benefit the scientific community and will serve as a reference for specialists and non-specialists interested in studying sea urchins.

Characterization of thyrotropin-releasing hormone producing neurons in sea urchin, from larva to juvenile

“…To follow the fate of the TRHergic cells during sea urchin larva development, IHC was performed on older larval stages. To describe the morphology of late P. lividus developmental stages, we used the detailed developmental atlas produced by Formery et al (2022) .…”

“…Nonetheless, examples of sea urchin lecithotrophic larvae, displaying direct development, also exist, even in the context of the same genus ( Raff, 1992 ), giving the opportunity to compare the two life cycle forms in closely related species ( Byrne et al, 2001 ; Katow et al, 2009 ). The morphology and development of planktotrophic sea urchins have been described in details from fertilization to metamorphosis by, among others ( Smith et al, 2008 ; Formery et al, 2022 ).…”

“…In contrast with the most studied sea urchin species S. purpuratus , in fact, P. lividus reaches metamorphosis in a relatively short time (about 1 month, compared to the roughly 3 months required for S. purpuratus ). A thorough description of P. lividus development from fertilization to metamorphosis was recently published by Formery et al (2022) and includes timing of all the stages. This gives us the possibility to study in detail how the sea urchin nervous system grows during the whole development and how the adult nervous system arises and connects to the larva nervous system.…”

Single-cell transcriptomics reveals evolutionary reconfiguration of embryonic cell fate specification in the sea urchinHeliocidaris erythrogramma

“…In contrast, the first indication of left-right asymmetry in the ancestral developmental mode occurs in the late gastrula (Duboc et al 2005; Bessodes et al 2012). Another accelerated patterning event in He involves the early establishment of the imaginal adult rudiment, which begins at about 30 hpf in He (Williams and Anderson 1975; Wray and Raff 1989; Koop et al 2017) but not until several days post-fertilization in the ancestral condition (Lowe et al 2002; Formery et al 2022).…”

See-Star: a versatile hydrogel-based protocol for clearing large, opaque and calcified marine invertebrates

“…See-Star is compatible with immunohistochemistry in diverse marine invertebrates Next, we tested whether See-Star was compatible with two of the most commonly used techniques for visualizing molecules, IHC and ISH. For IHC, we used a cross-reactive commercial anti-acetylated αtubulin antibody, which allows for visualization of neurons and cilia in a broad range of invertebrate species (Formery et al, 2022;Herranz et al, 2020;Martín-Durán & Hejnol, 2015;Rawlinson, 2010;Santagata et al, 2012;Schwaha et al, 2018;Zieger et al, 2018). We first assayed this antibody in cleared P. miniata post-metamorphic juveniles, defined by bearing only two pairs of secondary tube feet in each ray (2-TF stage) (Fig.…”