The Significance of Syncytial Tissues for the Position of the Hexactinellida in the Metazoa

Leys, Sally P.

doi:10.1093/icb/43.1.19

Cited by 68 publications

(25 citation statements)

References 55 publications

(22 reference statements)

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“…1C) have a very unusual structure with a syncytial body with partially isolated ''collar complexes'' instead of choanocytes (Mackie and Singla 1983;Leys 2003b). …”

Section: Evolution Of the Earliest Metazoans The Spongesmentioning

confidence: 99%

Six major steps in animal evolution: are we derived sponge larvae?

Nielsen¹

2008

Evolution and Development

255

259

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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.

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“…1C) have a very unusual structure with a syncytial body with partially isolated ''collar complexes'' instead of choanocytes (Mackie and Singla 1983;Leys 2003b). …”

Section: Evolution Of the Earliest Metazoans The Spongesmentioning

confidence: 99%

Six major steps in animal evolution: are we derived sponge larvae?

Nielsen¹

2008

Evolution and Development

255

259

View full text Add to dashboard Cite

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“…Thus, the identity of stem cells in these sponge groups is still an open question. In glass sponges, the presence of cells with archeocyte morphological features was reported based on electron microscopic studies (Leys, 2003;Leys et al, 2007). Demoponges are known to have archeocytes (totipotent somatic stem cells), which support both sexual and asexual reproduction.…”

Section: Introductionmentioning

confidence: 99%

The active stem cell specific expression of sponge Musashi homolog EflMsiA suggests its involvement in maintaining the stem cell state

Okamoto

Nakatsukasa²,

Alié

et al. 2012

Mechanisms of Development

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A hallmark of stem cells is the ability to sustainably generate stem cells themselves (self-renew) as well as differentiated cells. Although a full understanding of this ability will require clarifying underlying the primordial molecular and cellular mechanisms, how stem cells maintain their stem state and their population in the evolutionarily oldest extant multicellular organisms, sponges, is poorly understood. Here, we report the identification of the first stem cell-specific gene in demosponges, a homolog of Musashi (an evolutionarily conserved RNA binding protein that regulates the stem cell state in various organisms). EflMsiA, a Musashi paralog, is specifically expressed in stem cells (archeocytes) in the freshwater sponge Ephydatia fluviatilis. EflMsiA protein is localized predominantly in the nucleus, with a small fraction in the cytoplasm, in archeocytes. When archeocytes enter M-phase, EflMsiA protein diffuses into the cytoplasm, probably because of the breakdown of the nuclear membrane. In the present study, the existence of two types of M-phase archeocytes [(M)-archeocytes] was revealed by a precise analysis of the expression levels of EflMsiA mRNA and protein. In Type I (M)-archeocytes, presumably archeocytes undergoing self-renewal, the expression levels of EflMsiA mRNA and protein were high. In Type II (M)-archeocytes, presumably archeocytes committed to differentiate (committed archeocytes), the expression levels of EflMsiA mRNA and protein were about 60% and 30% lower than those in Type I (M)-archeocytes. From these results, archeocytes can be molecularly defined for the first time as EflMsiA-mRNA-expressing cells. Furthermore, these findings shed light on the mode of cell division of archeocytes and suggest that archeocytes divide symmetrically for both self-renewal and differentiation.

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“…They produce a skeleton of nearly pure glass (SiO 2 ) that can be >1 m in height and breadth; the major component of their soft tissue is a giant multinucleate syncytium, and although they have no nerves, they can propagate electrical signals through the whole organism to control their feeding current (Reiswig 1979, Mackie & Singla 1983, Leys & Mackie 1997, Leys 2003, Sandford 2003. These unusual features may reflect the ancient heritage of hexactinellids as the descendants of the earliest metazoans (Müller 2001), but it is also likely that they are adaptations of the sponges to their preferred deep-water habitat.…”

Section: Introductionmentioning

confidence: 99%

Patterns of glass sponge (Porifera, Hexactinellida) distribution in coastal waters of British Columbia, Canada

Leys

Wilson²,

Holeton³

et al. 2004

Mar. Ecol. Prog. Ser.

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Glass sponges are enigmatic members of the deep-sea fauna that inhabit shallow waters in only a few locations world-wide. In order to understand what factors influence the distribution of glass sponges, patterns of distribution and abundance of reef and non-reef forming hexactinellids in fjords of British Columbia, Canada, were analyzed from photographs and transcripts recorded on dives undertaken by the 'Pisces IV' manned submersible during the 1980s. Hexactinellids are widely distributed throughout all fjords from 16 to 650 m depths, and in some fjords abundances reach 240 individuals in 10 m 2 . In all fjords hexactinellids were most abundant at depths of 20 to 260 m, even where water depths exceeded 500 m. Glass sponges were rare in regions of inlets where oxygen levels fall below 2 ml l -1 , or in areas of high sediment deposition. Highest abundances coincided with water conditions of high dissolved silicate, low light, temperatures between 9 and 10°C and low suspended sediments. Extensive glass sponge skeletons in the inner basin of Howe Sound reflect past stress in this fjord that may include oxygen deficit, sediment loading from a mine and contamination from industrial sites. The observations from 'Pisces IV' suggest that glass sponges may be sentinel species for current and past seawater conditions in coastal British Columbia.

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The Significance of Syncytial Tissues for the Position of the Hexactinellida in the Metazoa

Cited by 68 publications

References 55 publications

Six major steps in animal evolution: are we derived sponge larvae?

Six major steps in animal evolution: are we derived sponge larvae?

The active stem cell specific expression of sponge Musashi homolog EflMsiA suggests its involvement in maintaining the stem cell state

Patterns of glass sponge (Porifera, Hexactinellida) distribution in coastal waters of British Columbia, Canada

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