Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes

Abstract

Abstract. Early development and metamorphosis of Reniera sp., a haplosclerid demosponge, have been examined to determine how gastrulation occurs in this species, and whether there is an inversion of the primary germ layers at metamorphosis. Embryogenesis occurs by unequal cleavage of blastomeres to form a solid blastula consisting micro‐ and macromeres; multipolar migration of the micromeres to the surface of the embryo results in a bi‐layered embryo and is interpreted as gastrulation. Polarity of the embryo is determined by the movement of pigment‐containing micromeres to one pole of the embryo; this pole later becomes the posterior pole of the swimming larva. The bi‐layered larva has a fully differentiated monociliated outer cell layer, and a solid interior of various cell types surrounded by dense collagen. The pigmented cells at the posterior pole give rise to long cilia that are capable of responding to environmental stimuli. Larvae settle on their anterior pole. Fluorescent labeling of the monociliated outer cell layer with a cell‐lineage marker (CMFDA) demonstrates that the monociliated cells resorb their cilia, migrate inwards, and transdifferentiate into the choanocytes of the juvenile sponge, and into other amoeboid cells. The development of the flagellated choanocytes and other cells in the juvenile from the monociliated outer layer of this sponge's larva is interpreted as the dedifferentiation of fully differentiated larval cells—a process seen during the metamorphosis of other ciliated invertebrate larvae—not as inversion of the primary germ layers. These results suggest that the sequences of development in this haplosclerid demosponge are not very different than those observed in many cnidarians.

Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans

“…First, the presumptive choanoderm cells (specified during early embryonic development) assume a peripheral position in the larvae. In the Amphimedon parenchymella, this process occurs by non-polarized cell migration, resulting in formation of the outer layer composed of small, ciliated cells, excluded from the posterior pole 60 . In the Sycon amphiblastula, the small ciliated cells move as an epithelial sheet through an opening between the macromeres (in the process referred to as inversion, eversion or excurvation) 30,37 .…”

Mini-opinion From unicellularity to multicellularity - molecular speculations about early animal evolution

“…Demosponges have been overlooked for developmental studies because their adult body plan appears simple and primitive, with little in common with the more advanced Metazoa (Brusca and Brusca, 2003). Only recently have embryogenesis and gastrulation shown startling similarities and homologies with other Metazoa (Leys, 2003a(Leys, ,b, 2004Leys and Degnan, 2002;Maldonado, 2004). Although adult sponges did not seem to have any obvious body axes, nor do they even have tissue-level organization, reassessment of their morphology proves that they possess rudimentary axes and cell types for tissue organization (Bavestrello et al, 1998;Borchiellini et al, 2001;BouryEsnault et al, 2003).…”

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

“…Twenty embryos at each of four developmental stages (white, beige, spot and ring stages, which cover early to late embryogenesis) were extracted from brood chambers as previously described (Leys and Degnan, 2002;Leys et al, 2008) and immediately frozen in a minimal volume of 0.22 µm-filtered seawater (FSW) at −80 • C for subsequent gDNA extraction.…”

“…It is particularly tractable for investigating host-symbiont interactions through the entire life cycle, as it houses asynchronously developing embryos and larvae through much of the year, in easily accessible brood chambers (Leys and Degnan, 2002;Degnan et al, 2005Degnan et al, , 2015Leys et al, 2008). It also is genome-enabled (Srivastava et al, 2010), facilitating investigations of molecular crosstalk between host and symbionts .…”