Integrating Complex Life Cycles in Comparative Developmental Biology.

The goal of comparative developmental biology is identifying mechanistic differences in embryonic development between different taxa and how these evolutionary changes have led to morphological and organizational differences in adult body plans. Much of this work has focused on direct-developing species in which the adult forms straight from the embryo and embryonic modifications have direct effects on the adult. However, most animal lineages are defined by indirect development, in which the embryo gives rise to a larval body plan and the adult forms by transformation of the larva. Historically, much of our understanding of complex life cycles is viewed through the lenses of ecology and zoology. In this review, we discuss the importance of establishing developmental rather than morphological or ecological criteria for defining developmental mode and explicitly considering the evolutionary implications of incorporating complex life cycles into broad developmental comparisons of embryos across metazoans.

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

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.

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

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.

Ambulacrarians and the Ancestry of Deuterostome Nervous Systems.

The evolutionary origin and history of metazoan nervous systems has been at the heart of numerous scientific debates for well over a century. This has been a particularly difficult issue to resolve within the deuterostomes, chiefly due to the distinct neural architectures observed within this group of animals. Indeed, deuterosomes feature central nervous systems, apical organs, nerve cords, and basiepidermal nerve nets. Comparative analyses investigating the anatomy and molecular composition of deuterostome nervous systems have nonetheless succeeded in identifying a number of shared and derived features. These analyses have led to the elaboration of diverse theories about the origin and evolutionary history of deuterostome nervous systems. Here, we provide an overview of these distinct theories. Further, we argue that deciphering the adult nervous systems of representatives of all deuterostome phyla, including echinoderms, which have long been neglected in this type of surveys, will ultimately provide answers to the questions concerning the ancestry and evolution of deuterostome nervous systems.

Pou3f transcription factor expression during embryonic development highlights distinct pou3f3 and pou3f4 localization in the Xenopus laevis kidney.

The POU (Pit-Oct-Unc) genes encode a large transcription factor family comprising 6 classes (pou1f to pou6f ) involved in many developmental processes, such as cell commitment and differentiation. The pou3f class contains four members (pou3f1, pou3f2, pou3f3, pou3f4) characterized by expression in ectodermal tissue derivatives, such as nervous system and otic vesicle, during mammalian development. In order to obtain insights into the potential conservation of this class of transcription factors in vertebrates, we carried out a phylogenetic analysis and a comprehensive comparative study of pou3f expression in the frog Xenopus laevis. All vertebrates examined possessed members of the four pou3f subfamilies, excepting the zebrafish, which lacked a pou3f4 gene. Whole mount in situ hybridization and real-time quantitative polymerase chain reaction (RT-qPCR) analyses revealed that Xenopus pou3f genes were expressed in the forming neural tube and their expression was maintained in the brain, mostly in the dorsal part, at tailbud stages. The pou3f2, pou3f3, and pou3f4 genes were also expressed in the developing otic vesicle, and pou3f1 in some cells of the epidermis. Besides ectodermal derivatives, pou3f3 and pou3f4 were expressed in the developing kidney. Their expression started at the early tailbud stage in the pronephric anlage and partly overlapped. In the mature pronephric tubule, pou3f3 was restricted to the intermediate tubule, while pou3f4 was also expressed in the distal and connecting tubule. Together, our results highlight a significant conservation of pou3f gene expression in vertebrates and indicate that they may have distinct but also redundant functions during neural and renal development.