Abstract
BackgroundThe 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.ResultsHere 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.ConclusionsOur 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.
Highlights
The evolutionary origin of gastrulation—defined as a morphogenetic event that leads to the establishment of germ layers—remains a vexing question
Sponges possess an internal network of canals and ciliated choanocyte chambers lined with epithelial cells, primarily endopinacocytes and choanocytes, and are separated from the external environment by another epithelial layer, the exopinacoderm
It was not determined whether all cell types found on the larval exterior are transdifferentiating at metamorphosis, and whether the larval epithelial cells differentiate directly into choanocytes or indirectly via an intermediate cell type
Summary
The evolutionary origin of gastrulation—defined as a morphogenetic event that leads to the establishment of germ layers—remains a vexing question. Sponges possess an internal network of canals and ciliated choanocyte chambers lined with epithelial cells, primarily endopinacocytes and choanocytes, and are separated from the external environment by another epithelial layer, the exopinacoderm (Figure 1; hexactinellids are constructed as a syncytium). Sandwiched between these epithelial layers is the collagenous mesohyl, which is enriched with multiple types of amoebocytes, including the pluripotent stem cell type, the archeocyte (Figure 1). Water currents created by ciliary beating in choanocyte chambers enable most of the physiological requirements of sponges, including feeding, respiration, excretion and reproduction This juvenile/ adult body plan is the outcome of the dramatic reorganisation of the radially-symmetrical, bi- or trilayered larva at metamorphosis [8]
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