New Insights into Placozoan Sexual Reproduction and Development

Abstract

Unraveling animal life cycles and embryonic development is basic to understanding animal biology and often sheds light on phylogenetic relationships. A key group for understanding the evolution of the Metazoa is the early branching phylum Placozoa, which has attracted rapidly increasing attention. Despite over a hundred years of placozoan research the life cycle of this enigmatic phylum remains unknown. Placozoa are a unique model system for which the nuclear genome was published before the basic biology (i.e. life cycle and development) has been unraveled. Four organismal studies have reported the development of oocytes and one genetic study has nourished the hypothesis of sexual reproduction in natural populations at least in the past. Here we report new observations on sexual reproduction and embryonic development in the Placozoa and support the hypothesis of current sexual reproduction. The regular observation of oocytes and expressed sperm markers provide support that placozoans reproduce sexually in the field. Using whole genome and EST sequences and additional cDNA cloning we identified five conserved sperm markers, characteristic for different stages in spermatogenesis. We also report details on the embryonic development up to a 128-cell stage and new ultrastructural features occurring during early development. These results suggest that sperm and oocyte generation and maturation occur in different placozoans and that clonal lineages reproduce bisexually in addition to the standard mode of vegetative reproduction. The sum of observations is best congruent with the hypothesis of a simple life cycle with an alternation of reproductive modes between bisexual and vegetative reproduction.

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

“…Notably absent from our developmental surveys below are data from placozoans. As there has been little advancement in efforts to spawn and successfully rear placozoan embryos through development [14], little is known about the spatial distribution of gene expression in these animals, and there is little opportunity to test hypotheses raised by the recent sequencing of the genome and proteome of Trichoplax adhaerens [15,16]. Conversely, there have been numerous recent advancements in our understanding of the evolution and development of diverse sponge taxa [17 -19].…”

Deep proteome profiling of Trichoplax adhaerens reveals remarkable features at the origin of metazoan multicellularity

“…It can be found in tropical and subtropical sea waters, and appears as a flat disc of 2-3 mm diameter consisting of two epithelial layers with a loose layer of fibre cells in between 5 . Trichoplax reproduces in vitro by fission and budding, and although in vitro the egg stadium does not develop into an embryonic stage beyond 64-128 cells, there are clear indications for a bisexual reproduction cycle, which left its signature in the DNA 6,7 . The Trichoplax genome contains 11,500 genes and, interestingly, includes importants genes characteristic of more complex bilaterian animals, such as developmental signalling pathways, neuroendocrine processes and extracellular matrix proteins 1 .…”

The most primitive metazoan animals, the placozoans, show high sensitivity to increasing ocean temperatures and acidities

“…At present, the phylum Placozoa is the only monotypic phylum in the animal kingdom, with the only formally described species Trichoplax adhaerens (Schulze, 1883, 1891). Placozoans offer unique possibilities for experimental ecophysiological studies because of their small size, simple morphology, and fast vegetative reproduction (Eitel & Schierwater, 2010; Eitel et al., 2011, 2013; Schierwater, 2005). Vegetative reproduction through binary fission or budding is the usual mode of reproduction in the laboratory and in the field.…”

“…Vegetative reproduction through binary fission or budding is the usual mode of reproduction in the laboratory and in the field. In contrast, bisexual reproduction is rarely seen in the laboratory, but most likely present in all placozoans (Eitel et al., 2011; Signorovitch, Buss, & Dellaporta, 2007). The details of sexual reproduction and embryonic development in placozoans remain widely unknown, because all efforts to complete the sexual life cycle in the laboratory have been unsuccessful, because embryonic development has never gone beyond the 128 cell stage (Eitel et al., 2011).…”

“…In contrast, bisexual reproduction is rarely seen in the laboratory, but most likely present in all placozoans (Eitel et al., 2011; Signorovitch, Buss, & Dellaporta, 2007). The details of sexual reproduction and embryonic development in placozoans remain widely unknown, because all efforts to complete the sexual life cycle in the laboratory have been unsuccessful, because embryonic development has never gone beyond the 128 cell stage (Eitel et al., 2011). As the overall effects of physiological stress are best seen in the performance of vegetative reproduction by binary fission, we used overall PGR as the dependent and easily quantifiable variable for the subsequent experiments.…”