Abstract
Poriferans (sponges) are sessile aquatic (largely marine) animals that are found in almost all benthic habitats. There are an estimated 15,000 species living today, although many have not been described (reviewed in Hooper and Van Soest 2002). The sponge body plan is amongst the simplest in the animal kingdom and lacks nerve and muscle cells and a centralised gut (reviewed in Simpson 1984; Ereskovsky 2010; Leys and Hill 2012). Their body plan and ecology, and thus their evolution, appear to be intimately associated with the diversity of microbial symbionts they harbour (reviewed in Hentschel et al. 2012; Thacker and Freeman 2012), as is the case with other metazoans.
Chapter vignette artwork by Brigitte Baldrian. © Brigitte Baldrian and Andreas Wanninger.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
Introduction
Poriferans (sponges) are sessile aquatic (largely marine) animals that are found in almost all benthic habitats. There are an estimated 15,000 species living today, although many have not been described (reviewed in Hooper and Van Soest 2002). The sponge body plan is amongst the simplest in the animal kingdom and lacks nerve and muscle cells and a centralised gut (reviewed in Simpson 1984; Ereskovsky 2010; Leys and Hill 2012). Their body plan and ecology, and thus their evolution, appear to be intimately associated with the diversity of microbial symbionts they harbour (reviewed in Hentschel et al. 2012; Thacker and Freeman 2012), as is the case with other metazoans (McFall et al. 2013).
Sponges are separated from the external environment by an epithelial layer, the exopinacoderm. External pores in this outer boundary connect to an internal network of canals and chambers, which are lined by epithelial endopinacocytes and ciliated choanocytes, respectively. Choanocyte chambers pump water through this internal aquiferous canal system, drawing food into the sponge. This current also fulfils most of the sponge’s physiological requirements, including respiration and excretion. Between the internal and external epithelial layers is the collagenous mesohyl, which is enriched with multiple cell types, often including pluripotent archaeocytes and skeletogenic sclerocytes that fabricate siliceous or calcareous spicules (Fig. 4.1). This juvenile/adult body plan is typically the outcome of the dramatic reorganisation of a radially symmetrical, bi- or trilayered larva at metamorphosis. Metamorphosis is deemed to be complete when the functional feeding juvenile is formed. This so-called rhagon or olynthus stage has been proposed to be the phylotypic stage for demosponges and calcisponges, respectively (reviewed in Ereskovsky 2010). It is often cited that poriferans lack true tissue-level organisation; however, there are numerous examples of tissue- and organ-like structures and functionalities in both larval and adult forms (e.g., the photosensitive pigment ring of many larvae).
Phylogenetic Position of Porifera
Porifera is traditionally regarded as the oldest surviving phyletic lineage of animals and in the past was often relegated into its own subkingdom, the Parazoa. Recent molecular phylogenetic analyses however have put forward a range of alternative proposals that either support (e.g., Philippe et al. 2009; Srivastava et al. 2010) or reject this traditional view (Fig. 4.2; e.g., Schierwater et al. 2009; Sperling et al. 2009; Ryan et al. 2013; Moroz et al. 2014). Specifically, current points of debate are whether poriferans or ctenophores are the sister group to all other animals and whether sponges are monophyletic. Thus, interpretations of the sponge body plan in the context of metazoan evolution range from it representing a state similar to the last common ancestor (LCA) of contemporary metazoans to it being derived from a morphologically more complex LCA that possessed a gut, nerves, and muscles.
Phylogenetic Relationships of Poriferan Classes
Classes Demospongiae, Calcarea, Homoscleromorpha, and Hexactinellida comprise phylum Porifera, with the Demospongiae being by far the most speciose. There is a growing consensus that demosponges and hexactinellids (sponges with a syncytial body organisation) and calcisponges and homoscleromorphs form pairs of sister classes (Fig. 4.3; Philippe et al. 2009; Gazave et al. 2012; Woerheide et al. 2012; Hill et al. 2013; Redmond et al. 2013; Thaker et al. 2013). However, there currently exist two broad views as to the exact relationship of these classes, one in which they form a monophyletic phylum (e.g., Philippe et al. 2009) and another where a clade comprised of demosponges and hexactinellids are separate from a clade comprised of calcisponges and homoscleromorphs + eumetazoans (Fig. 4.3; e.g., Sperling et al. 2009). Regardless, it appears that these classes diverged from each other over 600 million years ago, well before eumetazoan cladogenesis and the Cambrian explosion (Erwin et al. 2011).
Developmental Commonalities Within the Porifera
Poriferans exhibit a wide range of embryonic and larval types that are formed through a diversity of morphogenetic processes, many of which appear similar to those used during bilaterian development (Figs. 4.3 and 4.4). For instance, morphogenetic mechanisms, such as cell delamination (e.g., the hexactinellid Oopsacas minuta; Boury-Esnault et al. 1999), ingression (e.g., the halisarcid Halisarca dujardini; Gonobobleva and Ereskovsky 2004), egression (e.g., the homoscleromorph Oscarella sp.; Ereskovsky and Boury-Esnault 2002), and invagination (e.g., the halisarcid Halisarca dujardini; Gonobobleva and Ereskovsky 2004), are employed during sponge embryogenesis, albeit often in a taxon-restricted manner. For detailed descriptions of sponge development, the reader is directed to the recent excellent and scholarly book by Ereskovsky (2010) and other reviews (e.g., Leys 2004; Leys and Ereskovsky 2006; Leys and Hill 2012).
Regardless of the differences in external characteristics of different sponge embryos, larvae, postlarvae, juveniles, and adults (see Figs. 4.3 and 4.4), poriferan development employs a similar morphogenetic toolkit to that used by more complex animals. These fundamental features of development result from the spatiotemporal regulation of gene expression and include the establishment of differential cell affinities, cell type-specific movements, and structural changes and the regulation of cell proliferation and death. As we will see in later sections, the localised expression of transcription factor genes is likely to play a central role in establishing differential patterns of gene expression in sponges, just as it does in more complex animals. Further, mechanisms such as asymmetric cell division, cytoplasmic determinants, and intracellular signalling probably contribute to the specification and determination of cell identity in sponges. Other symmetry-breaking processes, such as morphogen gradients, also appear necessary for the formation of the poriferan body plan.
It is well accepted that multilayered poriferan body plans form through a series of morphogenetic processes underpinned by a combination of differential cell affinities and movements, but it remains a point of debate as to whether sponges gastrulate or possess germ layers (e.g., Leys 2004; Ereskovsky 2010; Leininger et al. 2014; Nakanishi et al. 2014). Perhaps less contentious, most morphogenetic movements in sponges can be viewed in the context of epithelial and mesenchymal cell behaviours and interactions. That is, during the course of development, sponge cells can operate semi-autonomously or in partially or fully integrated layers and have the capacity to migrate into or from a cell layer as an individual or a group (reviewed in Ereskovsky 2010).
With few exceptions, sponges have a biphasic pelagobenthic life cycle with a tiny, planktonic ciliated larva that metamorphoses and grows into a large, benthic adult that is sexually reproductive (Degnan and Degnan 2006, 2010; Ereskovsky 2010). The body plans of a majority of sponges continually undergo remodelling and regeneration throughout their life although this is less pronounced in some calcisponges (e.g., Sycon ciliatum). Thus, the morphogenetic mechanisms and processes outlined above, along with the processes of transdifferentiation and apoptosis, are operational throughout the life of most sponges (Ereskovsky 2010; Funayama 2012; Nakanishi et al. 2014). This also applies to asexual reproduction, which is not covered in this chapter.
The Demosponge Amphimedon queenslandica and the Calcareous Sponge Sycon ciliatum
As outlined above, sponge development is as varied as in any other phylum, and this chapter does not attempt to cover this diversity. Instead, here we focus on two species for which a majority of developmental gene expression patterns currently exist, the demosponge Amphimedon queenslandica and calcareous sponge Sycon ciliatum. Analysis of developmental gene expression, combined with experimental analysis of embryogenesis and metamorphosis, provides a means for more detailed and accurate comparisons of sponge and eumetazoan development. Both A. queenslandica and S. ciliatum have well-annotated draft genomes supported by extensive developmental transcriptomes (Srivastava et al. 2010; Anavy et al. 2014; Leininger et al. 2014). Importantly, these sponges differ markedly in their mechanisms of development. As demosponge and calcareous sponge lineages most likely diverged well before the Cambrian, a comparison of A. queenslandica and S. ciliatum genomes and development has the potential to provide insights into their common ancestor, which existed over 600 million years ago (Erwin et al. 2011).
The Demosponge Amphimedon queenslandica
Amphimedon queenslandica (class Demospongiae, order Haplosclerida, family Niphatidae) is currently the sponge with the most extensive developmental gene expression data. Its draft genome was published in 2010, further enhancing its utility for understanding demosponge development and metazoan evolution. A number of studies have been published about the evolution of metazoan cell types and gene families using A. queenslandica (Table 4.3). Akin to other sponges and indeed other animals, development in Amphimedon queenslandica progresses through a series of recognisable phases. It begins with the subdivision of the fertilised oocyte into progressively smaller blastomeres, followed by the acquisition of embryonic polarity and the sorting of cells into layers via broad-scale cell migrations. Activity then centres on the patterning and differentiation of diverse cell types in defined localities throughout the embryo and the morphogenesis of larval structures (Fig. 4.6). Differing from typical eumetazoan development in which patterning processes occur before terminal differentiation, embryonic pigment cells, ciliated epithelial cells, and sclerocytes in A. queenslandica express terminal differentiation characters, pigment granules, cilia, and spicules, respectively, directly following cleavage. Early differentiation of cells during embryogenesis appears to be a shared feature amongst many sponges.
The Amphimedon queenslandica Brood Chamber: Gametogenesis and Fertilisation
Amphimedon queenslandica is viviparous, and its embryos are concentrated into brood chambers, several of which can occur in a single adult all year round (Fig. 4.5). However, the developmental origins of its gametes are unknown. In other viviparous sponges, oocytes appear to differentiate from either archaeocytes or choanocytes (reviewed in Simpson 1984; Kaye 1990; Ereskovsky 2010). The engulfment of nutrient-laden nurse cells (also called trophocytes/spherulous cells; Simpson 1984; Ereskovsky 2010) is considered an important feature of oogenesis (e.g., Fell 1969; Saller and Weissenfels 1985). Pre-cleavage stages are known to reside at the edges of the brood chambers in A. queenslandica and can be identified by their translucent, smaller appearance and flattened shape in comparison to the more spherical and opaque embryos (Fig. 4.5; Leys and Degnan 2001; Adamska et al. 2010). Embryos and unhatched larvae are mixed and located more centrally in the brood chamber, with later stages tending to be towards the middle of the chamber. Developmental stages are identifiable and named by the presence and pattern of pigment cells, which first appear during cleavage: white stage embryos comprise a range of early cleavage stages; brown embryos have pigment cells distributed throughout the embryo and mark the transition from cleavage to the two-layered embryo; cloud stage appears after the anterior-posterior (AP) axis is established, with the pigment cells concentrating towards the future posterior pole; and spot to ring stages are identified by pigment cells concentrated at the posterior pole either as a spot or ring – ring stage follows spot stage – and characterised by morphogenesis of specific cell types and tissues (Fig. 4.6).
Like many sponges, Amphimedon queenslandica is a hermaphrodite that reproduces by spermcast spawning, followed by the apparent passive uptake by maternal adults of free spermatozoa from what is presumably a very dilute suspension in the water column. Genotyping of microsatellite loci with high allelic diversity (that together yield a combined paternal exclusion probability of 95 %) has revealed that up to 26 different paternal adults can be attributed to progeny being brooded by a single maternal adult at any particular time (Table 4.1). Near neighbours (within 4 m radius) can account for most of the fertilisations, but some progeny appear to be fathered by sperm sourced from a greater distance (Table 4.1). In any particular brood chamber, up to 30 % of white stage embryos appear to be of maternal origin only (i.e., unfertilised). However, as noted below, early cleaving embryos include a large number of maternal nurse cells, which eventually die. The import of these additional maternal genomes may prevent the detection of paternal microsatellite alleles in early embryos by increasing the ratio of maternal to paternal amplifiable DNA.
Although Amphimedon queenslandica fecundity is highest in the warmer months of the year, embryos of most developmental stages are present in most brood chambers at most times (Table 4.2). While overall there can be a large number of paternal contributors to fertilisation in a single maternal adult, only a subset of these fathers appear to contribute to any one brood chamber. There is no indication, however, that all embryos at a particular developmental stage within a brood chamber represent a single input of sperm from a single paternal source. Together, these observations suggest that A. queenslandica adults maintain a constant supply of all developmental stages, leading to a steady daily release of mature larvae (Maritz et al. 2010), by (i) passively accepting sperm that are trickle released continuously from neighbouring paternal adults and possibly also (ii) active regulation of fertilisation by stored sperm and/or regulation of the initiation or rate of development of fertilised eggs.
Early Embryonic Development in Amphimedon queenslandica
Cleavage
Cleaving Amphimedon queenslandica embryos (Figs. 4.7, 4.8, 4.9, and 4.10) are similar to other demosponge embryos (Fig. 4.4; Fell 1969; Saller and Weissenfels 1985; De Vos et al. 1991; Kaye and Reiswig 1991; Leys and Ereskovsky 2006; reviewed in Ereskovsky 2010). The entire embryo is enveloped in a layer of squamous follicle cells with large nuclei, presumably of maternal origin (Fig. 4.8; Leys and Degnan 2002). In early cleaving stages, the blastomeres are unequal in size and loaded with yolk that appears to be derived from nutritive maternal nurse cells (e.g., Fell 1969). These large blastomeres contain large quantities of smaller eosinophilic (thus protein-rich) bodies that appear to be derived from nurse cells undergoing programmed cell death, based on the presence of compact pyknotic nuclei with intensely basophilic staining (Fig. 4.8). Terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) – a method that detects fragmented DNA – of pyknotic nuclei in these bodies is consistent with these being derived from apoptosing nurse cells (Fig. 4.9A).
Blastomere cytoplasm appears as a thin layer around the mass of yolk-containing vesicles, with embryonic nuclei visible at the cell periphery (Fig. 4.8, black arrows). The extent of these yolk reserves means that neither blastomere cytoplasm nor cell boundaries are always apparent (Figs. 4.7 and 4.8; Leys and Degnan 2002). As cleavage progresses, the blastomeres reduce in size, and the number and concentration of pyknotic nuclei decreases (Figs. 4.9B and 4.10).
At the end of cleavage, a solid blastula forms, which is light brown in colour (Fig. 4.11). These ‘brown’ embryos contain a mixture of loosely aggregated cell types, of which six are readily identifiable: early sclerocytes around the outer margin of the embryo, two larger cell types with a variety of inclusions (designated here as type I and II macromeres), large amoeboid cells, pigment cells, and a minor micromere population (Fig. 4.11B–E). The type I and II macromeres are both spherulous and contain granular or homogenous inclusions, respectively. The amoeboid cells possess smaller and more lightly eosinophilic inclusions and larger nuclei with dense heterochromatin around their periphery. The early differentiation of some cell types, especially sclerocytes, occurs in a range of sponge embryos (Fell 1969; Maldonado and Berquist 2002; Leys 2003). Despite displaying characteristics of their final larval differentiated state (e.g., pigmentation, deposition of spicule matrix, ciliation), these cells remain to be patterned in the embryo and thus maintain the capacity to respond to positional signals and migrate appropriately.
Asymmetric Cell Division and Transcript Localisation
During cleavage an increasing number of small blastomeres are present on the periphery of the embryo and nestled between the macromeres. Following the fate of daughter cells originating from individual macromeres injected with high molecular weight tetramethylrhodamine dextran confirms that macromeres divide asymmetrically, giving rise to micromeres, typically 2–4 μm in diameter, and macromeres, initially most often >50 μm in diameter; symmetric cell divisions may occur in late cleavage (Fig. 4.12). The location of the daughter cells of individually labelled macromeres provides no evidence of stereotypical or predictable cell lineages or cleavage patterns. Instead, cleavage appears to be chaotic.
Morphologically distinct pigment cells, sclerocytes, and ciliated cells are first detected during cleavage throughout the embryo (Fig. 4.11; Leys and Degnan 2002). Consistent with the early specification and determination of these cell types is the detection of transcripts encoding a number of conserved developmental transcription factors in subpopulations of micromeres at cleavage, including NK homeobox genes Bsh and Tlx, LIM homeobox gene Lhx3/4, and the nuclear receptor gene NR1 (Fig. 4.13; Larroux et al. 2006, 2007; Fahey et al. 2008; Bridgham et al. 2010; Srivastava et al. 2010b).
Further analysis of Lhx3/4 mRNA localisation at cleavage reveals transcripts are not only present in individual micromeres but are also associated with the cortex of adjacent macromeres (Fig. 4.14). Macromere cortices and micromeres are enriched in microtubules (Fig. 4.15). Nuclei also localise to the macromere cortical region, consistent with these being regions of cell division. Asymmetric inheritance of cell fate determinants, in the form of localised mRNAs, is widespread in animal development (reviewed in Knoblich 2010; Medioni et al. 2012). This typically requires the localisation of particular mRNAs via cytoskeleton-mediated active transport to a defined cortical region of the cell. These results suggest that such a mechanism is operational during Amphimedon queenslandica cleavage and probably essential for the early specification and determination of micromere fate.
A more extensive survey of gene expression patterns in cleaving embryos indicates that the localisation of transcripts to subsets of micromeres is widespread in Amphimedon queenslandica (Fig. 4.16). The lack of similarity in many of the in situ hybridisation patterns is consistent with different transcripts being localised to different sets of micromeres; this suggests that cell fate specification and determination starts early in A. queenslandica embryogenesis. This mode of cell specification may be an important feature of the early development of many sponges with similar external embryological characteristics (cf. Ereskovsky 2010). In addition to various transcription factor mRNAs, transcripts that localise to micromeres at cleavage include those encoding components of conserved signalling pathways, innate immunity factors, structural proteins, and RNA-binding proteins and presumptive germ line factors. It is worth noting that the last group, which includes vasa, nanos, and PL10, displays transcript enrichment around a subset of micromeres (Fig. 4.16B′–D′).
Cell Layer Formation and Establishment of Axial Polarity
Cleavage is followed by a period of differential cell movement that sorts these different cell types into inner and outer layers (Fig. 4.6C, D), with ciliated cells, sclerocytes, and pigment cells being enriched in the outer portion of the embryo (Figs. 4.11 and 4.17; Leys and Degnan 2002). The inner cell mass (ICM) is primarily composed of large granular cells (Fig. 4.17). At this stage, cells appear mesenchyme-like, lacking robust cell junctions and being surrounded by a collagenous extracellular matrix (ECM) (Leys and Degnan 2002). After this initial sorting, cells continue migrating to become patterned along the anterior-posterior (AP) axis (Fig. 4.1; Leys and Degnan 2002; Degnan et al. 2005; Adamska et al. 2007a, 2010).
Tracing cells on the surface of embryos, by labelling with the fluorescent lipophilic dye DiI, confirms that early Amphimedon queenslandica embryos undergo extensive cellular rearrangements between late cleavage (brown stage) and the establishment of the AP axis (‘cloud’ and ‘spot’ stages) (Fig. 4.18; Adamska et al. 2010). Accordingly, the spacing between cells in cleavage and early brown stages probably reflects a lack of robust intercellular adhesion as well as a lack of extensive extracellular material. A similar event has been inferred to occur in embryos of Ephydatia prior to the differentiation of cell layers (De Vos et al. 1991). These broad cell movements represent morphogenesis via ‘differential centrifugal migration’ or ‘multipolar migration/delamination’ and commonly rely on cell sorting via the relative adhesive properties of each cell type (Leys and Ereskovsky 2006).
Just before the cloud stage, Amphimedon queenslandica embryos undergo compaction (Adamska et al. 2010), which may mark the culmination of the mass cell migratory events. This also coincides with stronger cell adhesion in the embryo and the increased density of ECM (Leys and Degnan 2002; Adamska et al. 2010). The increased density of cells and the appearance of ECM in the inner layer of the cloud stage (Fig. 4.17; Leys and Degnan 2002) support this timing and interpretation of events. External cells labelled with DiI at the cloud stage and later in development do not migrate to the same extent as cells labelled during cleavage and brown stages (Fig. 4.18), suggesting that the majority of the cells in the outer layer of the embryo reach their final embryonic territory by the end of the cloud stage (i.e., spot stage).
Localisation of Wnt and TGF-β Transcripts in the Early Embryo
The establishment of the bilayered embryo with AP axial polarity is preceded by the localisation of Wnt-expressing cells in the future posterior half of the embryo (Adamska et al. 2007a, 2010). These cells initially appear to be evenly distributed in the cleaving embryo and then appear to migrate posteriorly (Fig. 4.19). The mechanisms underlying the coalescing of these Wnt-expressing cells towards the future posterior side of the embryo remain unknown. It is yet to be determined if the Wnt pathway or another mechanism, such as signalling from the maternal follicle layer, directs the formation of the embryonic axis. Nonetheless, many of the components of the Wnt pathway also are expressed in cleaving embryos, usually in subsets of micromeres, or the surrounding follicle layer (Fig. 4.16; Adamska et al. 2007a, 2010), suggesting that some embryonic cells are competent to respond to the Wnt ligand.
A gene encoding a TGF-β ligand is expressed initially in a fraction of small cells distributed throughout the outer layer of the cleaving Amphimedon queenslandica embryo (Adamska et al. 2007a). During the formation of the bilayered embryo, transcripts become differentially localised along the AP axis and enriched at the poles (Fig. 4.19). These results are consistent with Wnt and TGF-β pathways working together to pattern the embryonic AP axis, from which will form the radially symmetrical A. queenslandica larva. During the formation of the cell layers and the establishment of the primary (AP) axis, many genes are differentially expressed in the inner and outer cell layers (Fig. 4.20).
In most eumetazoans, Wnt and TGF-β pathways are responsible for patterning of the AP and dorsoventral body axes (reviewed in Martindale 2005; see also Hayward et al. 2002; Matus et al. 2006). The differential expression of Wnt and TGF-β along the demosponge AP axis suggests that these genes were used to pattern the body plans of the first (radially symmetrical) animals (Adamska et al. 2007a, 2010).
Late Embryonic Development in Amphimedon queenslandica
In Amphimedon queenslandica, late embryonic development is considered to start at the spot stage, when the bi-layered embryo has an obvious AP axis and when the larval body plan is completely formed. In some cases, cells combine with other cells of the same type to form simple tissues, including the ciliated epithelium, the anterior cuboidal cell cluster, the pigment ring, and the ciliated ring. The latter two tissues combine to form a functional photosensory organ (Rivera et al. 2012).
Spot Stage and Commencement of Larval Tissue Formation
The early spot stage is characterised by the coalescence of the pigment cells at the posterior pole (Fig. 4.21A, B). Directly beneath the pigment spot, a dense group of type I macromeres remains, as seen in earlier stages, and the inner layer contains an increasing amount of extracellular material (Fig. 4.21C). The cell population at the anterior pole has formed a compact group (Fig. 4.21D). At the posterior, a group of columnar cells with an apical cilium and basal inclusions are aligned adjacent to the pigment spot (Fig. 4.21E, F).
In later spot stage embryos (Fig. 4.22A), a population of micromeres (non-pigmented) at the posterior pole becomes apparent; these form a ‘cap’ in the centre of the pigment spot (Fig. 4.22B). Directly opposite, the group of cells at the anterior pole is more condensed than previously (Fig. 4.22C). The outer epithelium of the embryo forms in a posterior to anterior progression (Fig. 4.22D), and the follicle layer separates from the embryo as the outer epithelium gains integrity (white arrows, Fig. 4.22D). Immediately adjacent to and anterior of the pigment spot is a population of ciliated epithelial cells (Fig. 4.22E). Immediately anterior to these, micromeres of the outer layer are lined up along the margin of the embryo and are thickened apically, forming a distinct boundary edge (Fig. 4.22F). Closer to the anterior pole, the micromeres of the outer layer are not organised into a distinct layer (Fig. 4.22G).
Pigment Ring Formation
The ring stage is identified by the wrinkled appearance of the embryo and the transformation of the pigment spot into a pigment ring at the posterior pole (Fig. 4.23A). Ring formation occurs via an increase in the non-pigmented cells found at the posterior pole and the migration of pigment cells from a central position at the posterior pole, to being more laterally located at the surface (Fig. 4.23B). In addition, the pigment cells are polarised, with the pigment granules located apically, and the nucleus assuming a basal position in each cell (Fig. 4.23C). Adjacent to the pigment cells, the posterior ciliated cells remain a distinct group, packed in a tight cluster to the exclusion of other cells in the outer layer (Fig. 4.23C). The cells at the anterior pole by now are organised into a single layer, with the nucleus assuming a more apical position in each cell (Fig. 4.23D, E).
The outer layer of the embryo is ciliated (except at the anterior and posterior poles), and, as a consequence, the follicle layer is no longer closely associated with the embryonic surface (e.g., Fig. 4.23D). The ciliated cells of the outer layer are polarised, with nuclei located basally and the apical region of each cell bearing a cilium (Fig. 4.23F, G). All macromeres have left the outer layer by this stage and are either located in the inner cell mass or at the boundary between the inner and outer layers (Fig. 4.23F). A new cell type – the flask cell (Leys and Degnan 2001) – is now identifiable amongst the ciliated epithelial cells towards the anterior of the embryo; they are ciliated with a centrally located nucleus and numerous small basally located vesicles (Fig. 4.23G). The inner layer of the embryo contains a diversity of unidentified cell types that are embedded in extracellular material (Fig. 4.23H). Numerous sclerocytes are also present (Fig. 4.23I).
The late ring embryo is elongated in comparison to earlier stages and is morphologically very similar to the larval form (Fig. 4.24A). At the posterior, the pigment cells are organised into a symmetrical ring around the pole with the apical region of each pigment cell protruding from the embryo (Fig. 4.24B). The posterior ciliated cells that lie adjacent to the pigment ring are also polarised, with basal nuclei, and the cells now appear to be clustered into small groups (Fig. 4.24B).
At the anterior pole, the cells are organised into a single layer and, in contrast to the surrounding epithelium, are non-ciliated (Fig. 4.24C). In the outer layer, which had previously been empty of macromeres, a population of globular cells (putatively derived from the type II macromere population) is now evident. These cells appear to migrate outwards from the forming subepithelial layer, through the outer layer to the periphery of the embryo (white arrows, Fig. 4.24D). A further group of globular macromeres is found at the posterior pole, within the ring of pigment cells (Fig. 4.24B). Between the ICM and the outer epithelium, a third cell layer – the subepithelial layer – is now evident; it is composed of spherulous cells interspersed with a number of smaller, unidentified cells (Fig. 4.24E). Cells of the ICM are positioned with their long axes aligned to the anterior-posterior axis of the embryo (Fig. 4.24F). The majority of sclerocytes are now located either within the ICM or at the boundary between the ICM and the subepithelial layer (not shown).
At this late stage, some cells combine with other cells of the same type to form simple tissues, including ciliated epithelium, anterior cuboidal cells, pigment ring cells, and ciliated ring cells. Pigment ring cells and ciliated ring cells combine to form a functional photosensory organ (Fig. 4.25). Figure 4.26 summarises the stages of Amphimedon queenslandica embryonic development, tracing the genesis of larval cell types.
Autonomous Formation of Pigment Spots and Rings
The formation of a pigment ring at the posterior end of the larva is essential to the photosensory capabilities of the larva (Leys and Degnan 2001; Rivera et al. 2012). The ring must be in a near-perfect circular pattern for the larva to swim away from light. The developmental mechanisms underlying the formation of this and other sponge tissues remain largely unknown.
Grafting of pigment cells from cloud, spot, and early ring stage embryos to another embryo results in the ectopic formation of pigment spots and rings in the new location (Fig. 4.27). These structures develop in accordance with the location from which they originated, and not the position to which they were transplanted, indicating that the fates of these cells (in larvae) have been determined earlier in development. The ability of these heterotopic grafts to form rings out of the normal spatial context suggests that the formation of pigment rings from spots relies on an intrinsic signalling system and that pigment cells of different ages – from cloud to early ring, at least – have self-organising ability to form an ectopic ring.
Localised and Cell Type-Specific Gene Expression in Late Stage Embryos and Larvae
Many of the genes studied to date in Amphimedon queenslandica are differentially expressed in specific cell types or cell layers in spot and ring stage embryos and swimming larvae. The reader is directed to specific publications for detailed descriptions of specific genes (Table 4.3). From late spot/early ring stage to the newly hatched larval stage can be considered a second phase of cell differentiation, which follows from the first phase comprising the formation of pigment cells, sclerocytes, and ciliated epithelial cells during cleavage (see above). These later developmental stages are typified by localised and cell type-restricted expression of transcription factor, signalling pathway, and structural genes (Fig. 4.28). This includes enrichment of innate immunity and neuronal genes in globular cells (Fig. 4.28H Sakarya et al. 2007; Gauthier and Degnan 2008; Richards et al. 2008; Gauthier et al. 2010) and epithelial genes in the larval epithelium (Fig. 4.28G Fahey and Degnan 2010); other outer layer cell types – anterior cuboidal and flask cells – have cell-specific gene expression patterns (Fig. 4.28D, F; e.g., Adamska et al. 2007a, 2010; Richards and Degnan 2012). Restricted expression patterns in the ICM are consistent with there being a number of cryptic cell types in this layer (e.g., Sox2 is expressed only in a subset of cells on the periphery of the inner cell mass; Fig. 4.28J).
Localised Expression of Conserved Developmental Genes During Pigment Ring Formation
The photosensory capabilities of the posterior pigment ring in the Amphimedon queenslandica larva requires the patterning of at least two cell types, the inner pigment cells and the surrounding long-ciliated cells (Figs. 4.6 and 4.26); other cell types that exist in this larval territory include a cell type that may contain both pigment and a long cilium. The expression of cryptochrome 2 (Cry2) in long-ciliated cells is consistent with these being able to detect light (Leys et al. 2002; Rivera et al. 2012). Presumably the pigment cells shade the Cry2-expressing cells and thereby attenuate the level of light hitting these cells. This in turn affects the behaviour of the long cilia by an unknown mechanism.
During the migration of the pigment cells to the posterior pole, and especially during spot and ring formation, a raft of signalling ligand and transcription factor genes are differentially expressed in this region (state of knowledge summarised in Fig. 4.29). In addition to Wnt and TGF-β, which are activated before spot formation (Fig. 4.19), Hedgling and two Delta ligands are differentially expressed in patterns overlapping with the pigment spot and with adjacent Cry2-expressing cells (Fig. 4.29A). Some expression patterns correspond to the boundaries between spot and Cry2-expressing (long-ciliated) cells (Hedgling and Delta4) and Cry2-expressing (long-ciliated) and surrounding epithelial cells (Hedgling and TGF-β), while others do not correspond perfectly to obvious morphological territories (Adamska et al. 2007a, b, 2010; Richards and Degnan 2012). The overlapping expression patterns of signalling ligands in Amphimedon queenslandica are reminiscent of many situations in eumetazoan development, suggesting that combinatorial signalling via Wnt, TGF-β, Hedgehog/Hedgling, and Notch pathways is a crown metazoan synapomorphy (reviewed in Adamska et al. 2011).
At this same developmental stage, a diversity of transcription factor genes are activated in the posterior pole (Fig. 4.28B). Many of these genes are expressed in Cry2-expressing cells, although some have broader patterns; some overlap directly with a given signalling ligand gene (Lhx3/4 and WntA) or with a combination of signalling ligand genes (POUI and WntA + TGF-β + Delta4). Of the conserved transcription factor genes expressed in the vicinity of the Cry2-expressing cells, most have eumetazoan orthologs involved in neurogenesis and sensory cell specification (Larroux et al. 2006; Larroux 2007; Richards et al. 2008; Adamska et al. 2010; Richards 2010; Richards and Degnan 2012; Srivastava et al. 2010b). Between spot and ring stages, the posterior expression patterns of many of these genes change, often into broader domains (Fig. 4.28B, C). Although the specific role of these developmental genes is currently unknown in Amphimedon queenslandica, their restricted expression in particular cell types is akin to many developmental events in eumetazoans.
Settlement and Metamorphosis in Amphimedon queenslandica
As is the case with embryogenesis, metamorphosis varies markedly between sponges, although a common set of morphogenetic mechanisms tend to be deployed, e.g., epithelial mesenchyme transition (EMT; see Ereskovsky 2010 for a systematic analysis of sponge metamorphosis).
Competent Amphimedon queenslandica larvae undergo rapid metamorphosis when they come in contact with an inductive environmental cue. Typically, larvae require at least 4 h of further development (at 24 °C) after emerging from the mother sponge before they are able to respond to this cue. During this time they are negatively phototactic (Leys and Degnan 2001; Leys et al. 2002), although during the first 2 h they can be observed on occasion swimming upwards towards the surface, which may facilitate dispersal (Degnan and Degnan 2010). A strong inductive cue is associated with the surface of live encrusting and articulated coralline algae (Degnan and Degnan 2010). Upon settling on the algae, larvae undergo a rapid and dramatic reorganisation of the body plan (Fig. 4.30). In Amphimedon queenslandica, a functional feeding juvenile is formed in about 3 days after the initiation of metamorphosis. As is the case with most other marine invertebrates, Amphimedon queenslandica exhibits variation between individual larvae in (i) the timing of the onset of developmental competence to be induced to settle and initiate metamorphosis, (ii) the period of negative photosensitivity, and (iii) the responsiveness to specific environmental cues (e.g., different algae) (Leys and Degnan 2001; Degnan and Degnan 2010).
Within hours of settling, the larva changes into an encrusting mat (Fig. 4.30C). Tracing different populations of labelled larval cells – epithelial, flask, and internal archaeocytes – through metamorphosis reveals that there is no constancy in larval and juvenile cell layers, with all larval cell types apparently capable of transdifferentiating into any juvenile cell type. There is also extensive programmed cell death of epithelial cells at metamorphosis (Fig. 4.31; Nakanishi et al. 2014). In other words, there appears to be no relationship between the cell layers established during embryogenesis and those produced at metamorphosis. In other sponges, the larval epithelial layer has been reported to shed entirely (Bergquist and Green 1977), to be phagocytised by archaeocytes (Meewis 1939; Misevic and Burger 1982, 1990), to differentiate into choanocytes through a non-ciliated amoebocyte intermediate (Amano and Hori 1993, 2001), or to directly differentiate into choanocytes without loss of cilia (Ereskovsky et al. 2007; reviewed in Ereskovsky 2010). Interestingly, the endomesoderm gene GATA is consistently expressed in the inner layer of both larvae and juveniles, despite the extensive reorganisation of the body plan at metamorphosis. Labeling of juvenile choanocytes reveals a further lack of cell layer and identity permanency, with these cells dedifferentiating into archaeocytes and transdifferentiating into a range of juvenile cell types, including the outer exopinacoderm (Nakanishi et al. 2014).
The Calcareous Sponge Sycon ciliatum
Although Amphimedon queenslandica serves as an excellent demosponge model in evolutionary and developmental biology research, the vast evolutionary distance between sponge lineages makes it necessary to include additional model species to represent the remaining lineages. Calcareous sponges have been intensively studied in the past centuries, and analysis of their development has significantly influenced evolutionary theory. For example, Ernst Haeckel coined the term gastrulation and formulated the Gastrea theory, after investigation of development and metamorphosis of a syconoid species from the class Calcaronea (Haeckel 1874; revisited by Leys and Eerkes-Medrano 2005). Sycon ciliatum, an abundant North East Atlantic calcaronean sponge, is now emerging as a calcisponge model species, with extensive sequence resources and protocols for gene expression utilised in a variety of studies (Adamska et al. 2011; Fortunato et al. 2012, 2014; Nosenko et al. 2013; Robinson et al. 2013; Sebé-Pedrós et al. 2013; Fortunato 2014; Leininger et al. 2014; Zakrzewski et al. 2014).
The adult specimens of Sycon ciliatum are barrel shaped and usually reach 5 cm in length and have a typical syconoid body organisation: choanocyte chambers arranged around the central atrium (Fig. 4.32A–C). As for all calcisponges, it is viviparous with embryogenesis occurring in the narrow mesohyl layer between the outer pinacoderm and the inner choanoderm (Figs. 4.32C and 4.33). The larva (‘amphiblastula’) is approximately 100 μm long and is transparent, except for pigment deposited within the basal (inner) tips of the micromeres (Fig. 4.32D). It is composed of two major cell types: the numerous micromeres comprising the anterior part of the larva have flagella, in contrast to the larger and less numerous macromeres at the posterior pole (Fig. 4.32A, D). In contrast to the rhagon, the putative phylotypic juvenile stage of demosponges, the calcisponge juvenile has only a single choanocyte chamber (Figs. 4.32A, E and 4.34) and is referred to as the olynthus (Ereskovsky 2010). S. ciliatum is one of the few sponge species that maintains radial symmetry throughout its life.
Recent and ongoing studies demonstrate significant differences in the content of developmental regulatory genes (i.e., the developmental toolkit) between Amphimedon queenslandica and Sycon ciliatum (Fortunato et al. 2012, 2014; Sebé-Pedrós et al. 2013; Fortunato 2014; Leininger et al. 2014). In a majority of cases, the genome of S. ciliatum contains more protein family members than A. queenslandica: 21 versus 3 Wnt ligands, 22 versus 8 TGF-β ligands (Leininger et al. 2014), and 7 versus 4 Sox transcription factors (Fortunato et al. 2012). In addition, S. ciliatum possesses several developmental genes that are absent from A. queenslandica, for example, Eyes absent (Fortunato et al. 2014). In other gene families, the two species share different paralogs with bilaterians: for example, T-box family genes Brachyury and Eomes are present in S. ciliatum, while Tbox4/5 and TboxPor are present in A. queenslandica (Sebé-Pedrós et al. 2013). This complex picture appears more consistent with multiple independent gene family expansions and gene losses in sponge lineages than with being simply explained by sponge paraphyly (Fortunato 2014).
Sycon ciliatum Development
Development of calcaronean sponges has several unique features, beginning with fertilisation that is assisted by specialised cells of the mother sponge, called carrier cells (reviewed in Ereskovsky 2010). The oocytes are positioned between the pinacocyte and choanocyte layers; choanocytes directly overlying the oocytes lose their collars and become accessory cells. As a sperm cell penetrates into one of the accessory cells, this cell becomes a carrier cell. The sperm cell inside of the carrier cell is referred to as a spermiocyst and is transferred into the oocyte to complete fertilisation (Fig. 4.33A). Intriguingly, while 100 % of Sycon ciliatum specimens collected in May in the Norwegian fjords contain oocytes and a majority of those collected over a few days in late May contained fertilisation complexes, spermatogenesis was not observed despite frequent sampling over several years (Leininger et al. 2014 and unpublished observations). The development that follows fertilisation is also semi-synchronous across the S. ciliatum population, with individual sponges ‘lagging behind’ no more than a few days. This leads to the release of larvae at the end of June and beginning of July (Leininger et al. 2014).
Embryogenesis of calcaronean sponges is well described on light and electron microscopy levels (Amano and Hori 1992, 1993; Franzen 1988; Eerkes-Medrano and Leys 2006; reviewed in Ereskovsky 2010). Early cleavage is highly stereotypic, and up to the eight-cell stage, the embryo has a rhomboid shape with all blastomeres positioned in the plane defined by the choanocyte and pinacocyte layers (Figs. 4.32A, 4.33B, 4.35C, and 4.36A, B, G, I, N). Cytoplasmic bridges are initially maintained between blastomeres (Figs. 4.33B, C, 4.35C, and 4.36A, B). Subsequent divisions result in formation of a cup-shaped ‘stomoblastula’ embryo, its opening communicating with an opening formed between the accessory cells. When cell differentiation is completed, the embryo is composed of three cell types: large, granular, non-ciliated macromeres adjacent to the choanocytes; smaller and more numerous micromeres, which have cilia pointing into the embryonic cavity; and four cruciform cells, which convey a unique tetra-radial symmetry to the embryos (Figs. 4.32A, 4.33D, E, and 4.36). The embryo then undergoes inversion, which will both translocate it into the radial chamber and position the cilia on the outer surface of the larva. During this stage, a small number of maternally derived cells crawl into the larval cavity (Figs. 4.32A, 4.33G, 4.35E, F, and 4.37A, I, D, E, M, O, P; Franzen 1988; Ereskovsky 2010; Leininger et al. 2014).
Larvae released in laboratory conditions swim close to the water surface during the first 12–24 h post spawning and subsequently begin to search for an appropriate substrate for settlement. During metamorphosis, the larva settles on the anterior pole; within minutes the ciliated cells of the anterior half undergo epithelial-to-mesenchymal transition and form the inner cell mass (Figs. 4.32A and 4.34A). In contrast, the macromeres maintain their epithelial organisation, completely enclose the micromeres, and become the pinacocytes of the forming juvenile. The cross cells and the maternal cells degenerate soon after settlement (Amano and Hori 1993). Sclerocytes differentiate quickly within the inner cell mass and spicule production starts approximately 12 h after settlement. A single choanocyte chamber forms, and the postlarva expands by increasing the volume of the chamber and thinning its walls, so they are finally composed of two epithelial layers – the outer pinacoderm and the inner choanoderm, with narrow mesohyl sparsely populated with sclerocytes and other not well-characterised cell types in between (Figs. 4.32A, 4.34B–D, and 4.35H–J). Finally, the osculum opens, and the juvenile sponge acquires ascon-level organisation with porocytes providing connections (ostia) between choanoderm and pinacoderm (Figs. 4.32A, E and 4.34E). As the asconoid body plan gives rise to the syconoid body plan during subsequent growth, choanocytes of the original choanocyte chamber become replaced with endopinacocytes in the region where radial chambers form. In terms of morphology and directionality of the water flow, the radial chambers are reminiscent of the original juvenile and can be treated as serially homologous to the olynthus (Manuel 2001; Leininger et al. 2014).
Extensive gene expression analyses, based on a combination of quantitative transcriptome analysis and in situ hybridisation studies, have provided important clues regarding the homology of cell types and body plans between sponges and eumetazoans. Several genes involved in specification of neuronal and sensory cells in cnidarians and bilaterians are expressed during differentiation of the cruciform cells, which are suggested to be the sensory cells of the calcaronean larvae (Tuzet 1973). These genes include SoxB, PaxB, SixC, Elav, Msi and Nanos, Hmx, and other NK-related homeobox transcription factors, as well as several components of the Wnt signalling pathway (Fig. 4.36; Fortunato et al. 2012, 2014; Fortunato 2014; Leininger et al. 2014). Genes involved in specification of the cnidarian and bilaterian endomesoderm are expressed in the embryonic micromeres (which give rise to the choanoderm) and choanoderm of the adult sponges. These include downstream components of the Wnt and TGF-β signalling pathways as well as Brachyury and GATA transcription factors (Fig. 4.37; Leininger et al. 2014). Finally, numerous Wnt and TGF-β ligands are expressed in the posterior region of the larvae and around the osculum of the adults, highly reminiscent of expression patterns observed in cnidarians and supporting homology of the larval and adult body axes as postulated by Haeckel (1870) (Fig. 4.37; Leininger et al. 2014).
Open Questions
-
Is Porifera monophyletic and the sister phylum to all other extant metazoans? Particularly intriguing is the inability to convincingly determine whether sponges or ctenophores are the earliest branching phyletic lineage. One of the standout features when comparing the Amphimedon queenslandica genome with ctenophore genomes is the remarkable similarity in developmental and other (e.g., neuronal) gene repertoires. Indeed, the gene content similarity between ctenophores and Amphimedon queenslandica might be greater than that between A. queenslandica and Sycon ciliatum.
-
How does sponge embryogenesis and metamorphosis relate to hallmarks of eumetazoan and bilaterian development, including gastrulation and germ layers?
-
Are the cell layers observed in sponges homologous to bilaterian germ layers, and if so, is the generative mechanism for the establishment of these layers conserved across the animal kingdom? Even amongst the co-authors of this chapter, there is no agreement. Regardless, it is clear there exists an ancient developmental gene toolkit that is still in use in all animals. This includes conserved signalling pathways whose differential expression contributes to define body plan axes and embryonic territories (e.g., Wnt, Notch) and transcription factors whose expression correlates with the establishment of a cell layer or type (e.g., GATA). The level at which these developmental similarities are homologous to eumetazoan processes remains an open question.
References
Adamska M, Degnan SM, Green KM, Adamski M, Craigie A, Larroux C, Degnan BM (2007a) Wnt and TGF-β expression in the sponge Amphimedon queenslandica and the origin of metazoan embryonic patterning. PLoS ONE 2:e1031
Adamska M, Matus DQ, Adamski M, Green K, Rokhsar DS, Martindale MQ, Degnan BM (2007b) The evolutionary origin of hedgehog proteins. Curr Biol 17:R836–R837
Adamska M, Larroux C, Adamski M, Green K, Lovas E, Koop D, Richards GS, Zwafink C, Degnan BM (2010) Structure and expression of conserved Wnt pathway components in the demosponge Amphimedon queenslandica. Evol Dev 12:492–518
Adamska M, Zwafink C, Green K, Degnan BM (2011) What sponges can tell us about the evolution of developmental processes. Zoology 114:1–10
Amano S, Hori I (1992) Metamorphosis of calcareous sponges. 1. Ultrastructure of free-swimming larvae. Invert Reprod Dev 21:81–90
Amano S, Hori I (1993) Metamorphosis of calcareous sponges. 2. Cell rearrangement and differentiation in metamorphosis. Invert Reprod Dev 24:13–26
Amano S, Hori I (2001) Metamorphosis of coeloblastula performed by multipotential larval flagellated cells in the calcareous sponge Leucosolenia laxa. Biol Bull 200:20–32
Anavy L, Levin M, Khair S, Nakanishi N, Fernandez-Valverde SL, Degnan BM, Yanai I (2014) BLIND ordering of large-scale transcriptomic developmental timecourses. Development 141:1161–1166
Bergquist PR, Green CR (1977) Ultrastructural-study of settlement and metamorphosis in sponge larvae. Cahiers Biol Mar 18:289–302
Boury-Esnault N, Efremova S, Bézac C, Vacelet J (1999) Reproduction of a hexactinellid sponge: first description of gastrulation by cellular delamination in the Porifera. Invert Reprod Dev 35:187–201
Bridgham JT, Eick GN, Larroux C, Deshpande K, Harms MJ, Gauthier ME, Ortlund EA, Degnan BM, Thornton JW (2010) Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor. PLoS Biol 8:e1000497
Degnan SM, Degnan BM (2006) The origin of the pelagobenthic metazoan life cycle: what’s sex got to do with it? Integr Comp Biol 46:683–690
Degnan SM, Degnan BM (2010) The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life cycle evolution. Phil Trans R Soc B 365:641–651
Degnan BM, Leys SP, Larroux C (2005) Sponge development and antiquity of animal pattern formation. Integr Comp Biol 45:335–341
De Vos L, Rutzler K, Boury-Esnault N, Donadey C, Vacelet J (1991) Atlas of sponge morphology. Smithsonian Institution Press, Washington D.C. 128 pp
Eerkes-Medrano DI, Leys SP (2006) Ultrastructure and embryonic development of a syconoid calcareous sponge. Invert Biol 125:177–194
Ereskovsky AV, Boury-Esnault N (2002) Cleavage pattern in Oscarella species (Porifera, Demospongiae, Homoscleromorpha): transmission of maternal cells and symbiotic bacteria. J Nat Hist 36:1761–1775
Ereskovsky A (2010) The comparative embryology of sponges. Springer, Netherlands
Ereskovsky AV, Tokina DB, Bezac C, Boury-Esnault N (2007) Metamorphosis of cinctoblastula larvae (Homoscleromorpha, Porifera). J Morphol 268:518–528
Erwin DH, Laflamme M, Tweedt SM, Sperling EA, Pisani D, Peterson KJ (2011) The Cambrian conundrum: early divergence and later ecological success in the early history of animals. Science 334:1091–1097
Fahey B (2011) Origin of animal epithelia: insights from the genome of the demosponge Amphimedon queenslandica. PhD Thesis The University of Queensland
Fahey B, Degnan BM (2010) Origin of animal epithelia: insights from the sponge genome. Evol Dev 12:601–617
Fahey B, Larroux C, Woodcroft BJ, Degnan BM (2008) Does the high gene density in the sponge NK homeobox gene cluster reflect limited regulatory capacity? Biol Bull 214:205–217
Fell PE (1969) The involvement of nurse cells in oogenesis and embryonic development in the marine sponge, Haliclona ecbasis. J Morph 127:133–150.
Fortunato SAV (2014) Gene loss, lineage specific expansions and dynamic expression of developmental transcription factors in calcareous sponges. PhD Thesis University of Bergen
Fortunato S, Adamski M, Bergum B, Guder C, Jordal S, Leininger S, Zwafink C, Rapp HT, Adamska M (2012) Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns. EvoDevo 23:142012
Fortunato S, Leininger S, Adamska M (2014) Evolution of the Pax-Six-Eya-Dach network: the calcisponge case study. EvoDevo 5:23
Fortunato S, Adamski M, Mendivil O, Leininger S, Liu J, Ferrier DEK, Adamska M. Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes. Nature 514:620–623
Franzen W (1988) Oogenesis and larval development of Scypha ciliata (Porifera, Calcarea). Zoomorphology 107:349–357
Funayama N (2012) The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells). Dev Genes Evol 223:23–38
Gauthier MEA (2010) Developing a sense of self: exploring the evolution of immune and allorecognition mechanisms in metazoans using the demosponge Amphimedon queenslandica. PhD Thesis The University of Queensland
Gauthier M, Degnan BM (2008) The transcription factor NF-κB in the sponge Amphimedon queenslandica: insights into the evolutionary origin of the Rel homology domain. Dev Genes Evol 218:23–32
Gauthier MEA, Du Pasquier L, Degnan BM (2010) The genome of the sponge Amphimedon queenslandica provides new perspectives into the origin of Toll-like and Interleukin1 receptor pathways. Evol Dev 12:519–533
Gazave E, Lapebie P, Ereskovsky AV, Vacelet J, Renard E, Cardenas P, Borchiellini C (2012) No longer demospongiae: homoscleromorpha formal nomination as a fourth class of Porifera. Hydrobiologia 687:3–10
Gonobobleva EL, Ereskovsky AV (2004) Metamorphosis of the larva of Halisarca dujardini (Demospongiae, Halisarcida). Bull Inst R Sci Nat.Belg 74:101–114
Haeckel E (1870). Ueber den Organismus der Schwame und ihre Verwndtschaft mit den Corallen. Jena Zeitsch Naturwiss 5:207–235
Haeckel E (1874) Die Gastrae Theorie, die phylogenetische Classification des Thierreichs und die Homologie der Keimblatter. Jena Zeitsch Naturwiss 8:1–55
Hayward DC, Samuel G, Pontynen PC, Catmull J, Saint R, Miller DJ, Ball EE (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo. Proc Natl Acad Sci USA 99:8106–8111
Hentschel U, Piel J, Degnan SM, Taylor MW (2012) Genomic insights into the marine sponge microbiome. Nature Rev Microbiol 10:641–654
Hill MS, Hill AL, Lopez J, Peterson KJ, Pomponi S, Diaz MC, Thacker RW, Adamska M, Boury-Esnault N, Cárdenas P, Chaves-Fonnegra A, Danka E, De Laine BO, Formica D, Hajdu E, Lobo-Hajdu G, Klontz S, Morrow CC, Patel J, Picton B, Pisani D, Pohlmann D, Redmond NE, Reed J, Richey S, Riesgo A, Rubin E, Russell Z, Rützler K, Sperling EA, di Stefano M, Tarver JE, Collins AG (2013) Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes. PLoS ONE 8:e50437
Hooper JNA, Van Soest RWM (eds) (2002) Systema Porifera, vol 1, A guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York, xlvii, 1708
Kaye HR (1990) Reproduction in West Indian commercial sponges: oogenesis, larval development, and behavior. In: new Perspectives in sponge biology. Rützler K, ed., Smithsonian Institution Press, Washington DC:161–169
Kaye HR, Reiswig HM (1991) Sexual reproduction in four Caribbean commercial sponges. II. Oogenesis and transfer of bacterial symbionts. lnvert Reprod Dev 19:1–11
Knoblich JA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849–860
Larroux C (2007) Genome content and developmental expression of transcription factor genes in the demosponge Amphimedon queenslandica: insights into the Ancestral Metazoan Developmental Program. PhD Thesis The University of Queensland
Larroux C, Fahey B, Liubicich D, Hinman VF, Gauthier M, Gongora M, Green K, Wörheide G, Leys SP, Degnan BM (2006) Developmental expression of transcription factor genes in a demosponge: insights into the origin of metazoan multicellularity. Evol Dev 8:150–173
Larroux C, Fahey B, Degnan SM, Adamski M, Rokhsar DS, Degnan BM (2007) The NK homeobox gene cluster predates the origin of Hox genes. Curr Biol 17:706–710
Leininger S, Adamski M, Bergum B, Guder C, Liu J, Laplante M, Bråte J, Hoffmann F, Fortunato S, Jordal S, Rapp HT, Adamska M (2014) Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans. Nat Commun 5:3905
Leys SP (2004) Gastrulation in sponges. In Gastrulation, From Cells to Embryo. Edited by Stern CD. New York: cold Spring Harbor Laboratory Press:23–31
Leys SP, Degnan BM (2001) The cytological basis of photoresponsive behavior in a sponge larva. Biol Bull 201:323–338
Leys SP, Degnan BM (2002) Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invert Biol 121:171–189
Leys SP, Eerkes-Medrano D (2005) Gastrulation in calcareous sponges: in search of Haeckel’s gastraea. Integ Comp Biol 45:342–351
Leys SP, Ereskovsky AV (2006) Embryogenesis and larval differentiation in sponges. Can. J. Zool. 84:262–287
Leys SP, Hill A (2012) The physiology and molecular biology of sponge tissues. Adv Mar Biol 62:1–56
Leys SP, Cronin TW, Degnan BM, Marshall JN (2002) Spectral sensitivity in a sponge larva. J Comp Physiol A 188:199–202
Maldonado M, Bergquist PR (2002) Phylum Porifera. In: atlas of marine invertebrate larvae. Young CM, ed, Academic press, London:21–50
Manuel M (2001) Origine et évolution des mécanismes moléculaires contrôlant la morphogenèse chez les Métazoaires: un nouveau modèle spongiaire, Sycon raphanus (Calcispongia, Calcaronea). PhD Thesis Université de Paris XI
Maritz K, Calcino A, Fahey B, Degnan BM, Degnan SM (2010) Remarkable consistency of larval supply in the spermcast-mating demosponge Amphimedon queenslandica (Hooper and van Soest). Open Mar Biol J 4:57–64
Matus DQ, Pang K, Marlow H, Dunn CW, Thomsen GH, Martindale MQ (2006) Molecular evidence for deep evolutionary roots of bilaterality in animal development. Proc Natl Acad Sci USA 103:11195–11200
McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236
Medioni C, Mowry K, Besse F (2012) Principles and roles of mRNA localization in animal development. Development 139:3263–3276
Meewis H (1939) Contribution a l’étude de l’embryogenése de Chalinulidae: haliclona limbata. Ann Soc R Zool Belg 70:201–243
Misevic GN SV, Burger MM (1990) Larval metamorphosis of Microciona prolifera: evidence against the reversal of layers. In: Rt K (ed) New perspectives in sponge biology. Smithsonian Institution Press, Washington, DC, pp 182–187
Misevic GN, Burger MM (1982) The molecular basis of species specific cell-cell recognition in marine sponges, and a study on organogenesis during metamorphosis. Prog Clin Biol Res B 85:193–209
Moroz LL, Kocot KM, Citarella MR, Dosung S, Norekian TP, Povolotskaya IS, Grigorenko AP, Dailey C, Berezikov E, Buckley KM, Ptitsyn A, Reshetov D, Mukherjee K, Moroz TP, Bobkova Y, Yu F, Kapitonov VV, Jurka J, Bobkov YV, Swore JJ, Girardo DO, Fodor A, Gusev F, Sanford R, Bruders R, Kittler E, Mills CE, Rast JP, Derelle R, Solovyev VV, Kondrashov FA, Swalla BJ, Sweedler JV, Rogaev EI, Halanych KM, Kohn AB (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510:109–114
Nakanishi N, Sogabe S, Degnan BM (2014) Evolutionary origin of gastrulation: insights from sponge development. BMC Biol 12:26
Nosenko T, Schreiber F, Adamska M, Adamski M, Eitel M, Hammel J, Maldonado M, Müller WE, Nickel M, Schierwater B, Vacelet J, Wiens M, Wörheide G (2013) Deep metazoan phylogeny: when different genes tell different stories. Mol Phylogenet Evol 67:223–233
Philippe H, Derelle R, Lopez P, Pick K, Borchiellini C, Boury-Esnault N, Vacelet J, Renard E, Houliston E, Quéinnec E, Da Silva C, Wincker P, Le Guyader H, Leys S, Jackson DJ, Schreiber F, Erpenbeck D, Morgenstern B, Wörheide G, Manuel M (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:706–712
Redmond NE, Morrow CC, Thacker RW, Diaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lôbo-Hajdu G, Picton BE, Pomponi SA, Kayal E, Collins AG (2013) Phylogeny and systematics of Demospongiae in light of new small-subunit ribosomal DNA (18S) sequences. Integ Comp Biol 53:388–415
Richards GS (2010) The origins of cell communication in the animal kingdom: notch signalling during embryogenesis and metamorphosis of the demosponge Amphimedon queenslandica. PhD Thesis The University of Queensland
Richards GS, Degnan BM (2012) The expression of Delta ligands in the sponge Amphimedon queenslandica suggests an ancient role for Notch signaling in metazoan development. EvoDevo 3:e15
Richards GS, Simionato E, Perrron M, Adamska M, Vervoort M, Degnan BM (2008) Sponge genes provide new insight into the evolutionary origin of the neurogenic circuit. Curr Biol 18:1156–1161
Rivera AS, Ozturk N, Fahey B, Plachetzki DC, Degnan BM, Sancar A, Oakley TH (2012) Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin. J Exp Biol 215:1278–1286
Robinson JM, Sperling EA, Bergum B, Adamski M, Nichols SA, Adamska M, Peterson KJ (2013) The identification of microRNAs in calcisponges: independent evolution of microRNAs in basal metazoans. J Exp Zool B Mol Dev Evol 320:84–93
Ryan JF, Pang K, Schnitzler CE, Nguyen AD, Moreland RT, Simmons DK, Koch BJ, Francis WR, Havlak P, NISC Comparative Sequencing Program, Smith SA, Putnam NH, Haddock SH, Dunn CW, Wolfsberg TG, Mullikin JC, Martindale MQ, Baxevanis AD (2013) The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342:1242592
Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, Degnan BM, Oakley TH, Kosik KS (2007) A post-synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2:e506
Saller U, Weissenfels N (1985) The development of Spongilla lacustris from the oocyte to the free larva (Porifera, Spongillidae). Zoomorph 105:252–277
Schierwater B, Eitel M, Jakob W (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol 7:e20
Sebé-Pedrós A, Ariza-Cosano A, Weirauch MT, Leininger S, Yang A, Torruella G, Adamski M, Adamska M, Hughes TR, Gómez-Skarmeta JL, Ruiz-Trillo I (2013) Early evolution of the T-box transcription factor family. Proc Natl Acad Sci U S A 110:16050–16055
Simpson TL (1984) The cell biology of sponges. Springer, New York
Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol 26:2261–2274
Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010a) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–726
Srivastava M, Larroux C, Lu DR, Mohanty K, Chapman J, Degnan BM, Rokhsar DS (2010b) Early evolution of the LIM homeobox gene family. BMC Biol 8:e4
Steinmetz PRH, Kraus JEM, Larroux C, Hammel JU, Amon-Hassenzahl A, Houliston E, Wörheide G, Nickel M, Degnan BM, Technau U (2012) Independent evolution of striated muscles in cnidarians and bilaterians. Nature 487:231–234
Thacker RW, Freeman CJ (2012) Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol 62:57–111
Thacker RW, Hill AL, Hill MS, Redmond NE, Collins AG, Morrow CC, Spicer L, Carmack CA, Zappe ME, Pohlmann D, Hall C, Diaz MC, Bangalore PV (2013) Nearly complete 28S rRNA gene sequences confirm new hypotheses of sponge evolution. Integ Comp Biol 53:373–387
Tuzet O (1973) Éponges calcaires. In: Grassé P-P (ed) Traité de Zoologie Anatomie, Systématique, Biologie Spongiaires, vol 3. Masson et Cie, Paris, pp 27–132
Worheide G, Dohrmann M, Erpenbeck D, Larroux C, Maldonado M, Voigt O, Borchiellini C, Lavrov DV (2012) Deep phylogeny and evolution of sponges (phylum Porifera). Adv Mar Biol 61:1–78
Zakrzewski A-C, Weigert A, Helm C, Adamski M, Adamska M, Bleidorn C, Raible F, Hausen H (2014) Early divergence, broad distribution and high diversity of animal chitin synthases. Genome Biol Evol 6:316–325
Acknowledgements
Because of space limitations, we are unable to cite many important contributions to the field of sponge developmental biology – we acknowledge these here. We also acknowledge the fine contributions of past and present members of the laboratories of B. Degnan, S. Degnan, and M. Adamska towards our understanding of Amphimedon and Sycon biology. Research presented in this chapter was made possible by the generous support of the Australian Research Council to BMD, SMD, and MA and the Sars International Centre for Marine Molecular Biology to MA.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer-Verlag Wien
About this chapter
Cite this chapter
Degnan, B.M. et al. (2015). Porifera. In: Wanninger, A. (eds) Evolutionary Developmental Biology of Invertebrates 1. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1862-7_4
Download citation
DOI: https://doi.org/10.1007/978-3-7091-1862-7_4
Publisher Name: Springer, Vienna
Print ISBN: 978-3-7091-1861-0
Online ISBN: 978-3-7091-1862-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)