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The evolutionary origin of metazoan cell types such as neurons and muscles is not known. Using whole-body single-cell RNA sequencing in a sponge, an animal without nervous system and musculature, we identified 18 distinct cell types. These include nitric oxide–sensitive contractile pinacocytes, amoeboid phagocytes, and secretory neuroid cells that reside in close contact with digestive choanocytes that express scaffolding and receptor proteins. Visualizing neuroid cells by correlative x-ray and electron microscopy revealed secretory vesicles and cellular projections enwrapping choanocyte microvilli and cilia. Our data show a communication system that is organized around sponge digestive chambers, using conserved modules that became incorporated into the pre- and postsynapse in the nervous systems of other animals.

A hallmark of metazoan evolution is the emergence of genomic mechanisms that implement cell-type-specific functions. However, the evolution of metazoan cell types and their underlying gene regulatory programmes remains largely uncharacterized. Here, we use whole-organism single-cell RNA sequencing to map cell-type-specific transcription in Porifera (sponges), Ctenophora (comb jellies) and Placozoa species. We describe the repertoires of cell types in these non-bilaterian animals, uncovering diverse instances of previously unknown molecular signatures, such as multiple types of peptidergic cells in Placozoa. Analysis of the regulatory programmes of these cell types reveals variable levels of complexity. In placozoans and poriferans, sequence motifs in the promoters are predictive of cell-type-specific programmes. By contrast, the generation of a higher diversity of cell types in ctenophores is associated with lower specificity of promoter sequences and the existence of distal regulatory elements. Our findings demonstrate that metazoan cell types can be defined by networks of transcription factors and proximal promoters, and indicate that further genome regulatory complexity may be required for more diverse cell type repertoires.

Recent phylogenomic evidence suggests that ctenophores may be the sister group to the rest of animals. This phylogenetic arrangement opens the possibility that sponges and placozoans could have lost neural cell types or that the ctenophore nervous system evolved independently. We critically review evidence to date that has been put forth in support of independent evolution of neural cell types in ctenophores. We observe a reluctance in the literature to consider a lost nervous system in sponges and placozoans and suggest that this may be due to historical bias and the commonly misconstrued concept of animal complexity. In support of the idea of loss (or modification beyond recognition), we provide hypothetical scenarios to show how sponges and placozoans may have benefitted from the loss and/or modification of their neural cell types., (© 2015 The Author(s).)

Background: The evolutionary origin of gastrulation--defined as a morphogenetic event that leads to the establishment of germ layers--remains a vexing question. Central to this debate is the evolutionary relationship between the cell layers of sponges (poriferans) and eumetazoan germ layers. Despite considerable attention, it remains unclear whether sponge cell layers undergo progressive fate determination akin to eumetazoan primary germ layer formation during gastrulation., Results: Here we show by cell-labelling experiments in the demosponge Amphimedon queenslandica that the cell layers established during embryogenesis have no relationship to the cell layers of the juvenile. In addition, juvenile epithelial cells can transdifferentiate into a range of cell types and move between cell layers. Despite the apparent lack of cell layer and fate determination and stability in this sponge, the transcription factor GATA, a highly conserved eumetazoan endomesodermal marker, is expressed consistently in the inner layer of A. queenslandica larvae and juveniles., Conclusions: Our results are compatible with sponge cell layers not undergoing progressive fate determination and thus not being homologous to eumetazoan germ layers. Nonetheless, the expression of GATA in the sponge inner cell layer suggests a shared ancestry with the eumetazoan endomesoderm, and that the ancestral role of GATA in specifying internalised cells may antedate the origin of germ layers. Together, these results support germ layers and gastrulation evolving early in eumetazoan evolution from pre-existing developmental programs used for the simple patterning of cells in the first multicellular animals.

The emergence of multicellularity is regarded as one of the major evolutionary events of life. This transition unicellularity/pluricellularity was acquired independently several times (King 2004). The acquisition of multicellularity implies the emergence of cellular cohesion and means of communication, as well as molecular mechanisms enabling the control of morphogenesis and body plan patterning. Some of these molecular tools seem to have predated the acquisition of multicellularity while others are regarded as the acquisition of specific lineages. Morphogenesis consists in the spatial migration of cells or cell layers during embryonic development, metamorphosis, asexual reproduction, growth, and regeneration, resulting in the formation and patterning of a body. In this paper, our aim is to review what is currently known concerning basal metazoans--sponges' morphogenesis from the tissular, cellular, and molecular points of view--and what remains to elucidate. Our review attempts to show that morphogenetic processes found in sponges are as diverse and complex as those found in other animals. In true epithelial sponges (Homoscleromorpha), as well as in others, we find similar cell/layer movements, cellular shape changes involved in major morphogenetic processes such as embryogenesis or larval metamorphosis. Thus, sponges can provide information enabling us to better understand early animal evolution at the molecular level but also at the cell/cell layer level. Indeed, comparison of molecular tools will only be of value if accompanied by functional data and expression studies during morphogenetic processes.

The first animals arose more than six hundred million years ago, yet they left little impression in the fossil record. Nonetheless, the cell biology and genome composition of the first animal, the Urmetazoan, can be reconstructed through the study of phylogenetically relevant living organisms. Comparisons among animals and their unicellular and colonial relatives reveal that the Urmetazoan likely possessed a layer of epithelium-like collar cells, preyed on bacteria, reproduced by sperm and egg, and developed through cell division, cell differentiation, and invagination. Although many genes involved in development, body patterning, immunity, and cell-type specification evolved in the animal stem lineage or after animal origins, several gene families critical for cell adhesion, signaling, and gene regulation predate the origin of animals. The ancestral functions of these and other genes may eventually be revealed through studies of gene and genome function in early-branching animals and their closest non-animal relatives.

In the last 15 years, we had to cope with many technological and conceptual obstacles. The major hindrance was the view that sponges are primitive and exist separated from the other metazoan organisms. After answering these problems, the painful scientific process to position the most enigmatic metazoan phylum, the Porifera, into the correct phylogenetic place among the eukaryotes in general and the multicellular animals in particular came to an end. The well-studied taxon Porifera (sponges) was first grouped to the animal-plants or plant-animals, then to the Zoophyta or Mesozoa, and finally to the Parazoa. Only by the application of molecular biological techniques was it possible to place the Porifera monophyletically with the other metazoan phyla, justifying a unification of all multicellular animals to only one kingdom, the Metazoa. The first strong support came from the discovery that cell-cell and cell-matrix adhesion molecules, that were cloned from sponges (mainly the demosponges Suberites domuncula and Geodia cydonium) and that were subsequently expressed, share high DNA sequence and protein function similarity with the corresponding molecules of other metazoans. Together with the molecular biological studies and with the use of the cell culture technologies (primmorphs), which allowed an insight into the stem cell system of these simple organisms, it was possible to stethoscope back in the paleontological history of animals. These studies confirmed the view that the sponges evolved between two epochal ice times, 710-680 Ma (Sturtian glaciation) and 605-585 Ma (Varanger-Marinoan ice age), a period which allowed evolution to proceed but resulted also in a mass extinction of most animal taxa, with the exception of the Porifera. These animals could develop in the aqueous milieu which was rich in silica, due also to their ability to live in a symbiosis with unicellular organisms (prokaryotic and also eukaryotic). Those organisms provided the sponges with the nutrition to survive and to overcome the food deprivation in cold water and even in an environment under the ice. Based on the diverse genetic toolkit, the sponges could also resist the adverse temperature and sunlight climatic influences. It is fortunate that the sponges survived the last 800 million years with their basic body plan. This fact might qualify the sponges to become model organisms not only in biology and molecular biology but also to be used - as living fossils - as reference organisms to deduce important and new insights in the understanding of fossil records explored from the Neoproterozoic. Taken together, these data caused a paradigmatic change; the Porifera are complex and simple, but by far not primitive, and they contribute to the understanding of the deep evolution of animals in molecular biological and paleontological views.

We know little about the genomic events that led to the advent of a multicellular grade of organization in animals, one of the most dramatic transitions in evolution. Metazoan multicellularity is correlated with the evolution of embryogenesis, which presumably was underpinned by a gene regulatory network reliant on the differential activation of signaling pathways and transcription factors. Many transcription factor genes that play critical roles in bilaterian development largely appear to have evolved before the divergence of cnidarian and bilaterian lineages. In contrast, sponges seem to have a more limited suite of transcription factors, suggesting that the developmental regulatory gene repertoire changed markedly during early metazoan evolution. Using whole-genome information from the sponge Amphimedon queenslandica, a range of eumetazoans, and the choanoflagellate Monosiga brevicollis, we investigate the genesis and expansion of homeobox, Sox, T-box, and Fox transcription factor genes. Comparative analyses reveal that novel transcription factor domains (such as Paired, POU, and T-box) arose very early in metazoan evolution, prior to the separation of extant metazoan phyla but after the divergence of choanoflagellate and metazoan lineages. Phylogenetic analyses indicate that transcription factor classes then gradually expanded at the base of Metazoa before the bilaterian radiation, with each class following a different evolutionary trajectory. Based on the limited number of transcription factors in the Amphimedon genome, we infer that the genome of the metazoan last common ancestor included fewer gene members in each class than are present in extant eumetazoans. Transcription factor orthologues present in sponge, cnidarian, and bilaterian genomes may represent part of the core metazoan regulatory network underlying the origin of animal development and multicellularity.

A review of the old and new literature on animal morphology/embryology and molecular studies has led me to the following scenario for the early evolution of the metazoans. The metazoan ancestor, "choanoblastaea," was a pelagic sphere consisting of choanocytes. The evolution of multicellularity enabled division of labor between cells, and an "advanced choanoblastaea" consisted of choanocytes and nonfeeding cells. Polarity became established, and an adult, sessile stage developed. Choanocytes of the upper side became arranged in a groove with the cilia pumping water along the groove. Cells overarched the groove so that a choanocyte chamber was formed, establishing the body plan of an adult sponge; the pelagic larval stage was retained but became lecithotrophic. The sponges radiated into monophyletic Silicea, Calcarea, and Homoscleromorpha. Homoscleromorph larvae show cell layers resembling true, sealed epithelia. A homoscleromorph-like larva developed an archenteron, and the sealed epithelium made extracellular digestion possible in this isolated space. This larva became sexually mature, and the adult sponge-stage was abandoned in an extreme progenesis. This eumetazoan ancestor, "gastraea," corresponds to Haeckel's gastraea. Trichoplax represents this stage, but with the blastopore spread out so that the endoderm has become the underside of the creeping animal. Another lineage developed a nervous system; this "neurogastraea" is the ancestor of the Neuralia. Cnidarians have retained this organization, whereas the Triploblastica (Ctenophora+Bilateria), have developed the mesoderm. The bilaterians developed bilaterality in a primitive form in the Acoelomorpha and in an advanced form with tubular gut and long Hox cluster in the Eubilateria (Protostomia+Deuterostomia). It is indicated that the major evolutionary steps are the result of suites of existing genes becoming co-opted into new networks that specify new structures. The evolution of the eumetazoan ancestor from a progenetic homoscleromorph larva implies that we, as well as all the other eumetazoans, are derived sponge larvae.

The review considers Ca2+ -messenger systems in primitive multicellulars (sponges and hydrozoa organisms). Analysis is performed of Ca2+ participation in regulation of early development of the organisms, their mobility, metamorphosis, chemoreception, and some other functions.

Demosponges are considered part of the most basal evolutionary lineage in the animal kingdom. Although the sponge body plan fundamentally differs from that of other metazoans, their development includes many of the hallmarks of bilaterian and eumetazoan embryogenesis, namely fertilization followed by a period of cell division yielding distinct cell populations, which through a gastrulation-like process become allocated into different cell layers and patterned within these layers. These observations suggest that the last common ancestor (LCA) to all living animals was developmentally more sophisticated than is widely appreciated and used asymmetric cell division and morphogen gradients to establish localized populations of specified cells within the embryo. Here we demonstrate that members of a range of transcription factor gene classes, many of which appear to be metazoan-specific, are expressed during the development of the demosponge Reniera, including ANTP, Pax, POU, LIM-HD, Sox, nuclear receptor, Fox (forkhead), T-box, Mef2, and Ets genes. Phylogenetic analysis of these genes suggests that not only the origin but the diversification of some of the major developmental metazoan transcription factor classes took place before sponges diverged from the rest of the Metazoa. Their expression during demosponge development suggests that, as in today's sophisticated metazoans, these genes may have functioned in the regulatory network of the metazoan LCA to control cell specification and regionalized gene expression during embryogenesis.