Placozoa – no longer a phylum of one

More than a century ago, the simplest of all metazoans was discovered and described as Trichoplax adhaerens [1]. These tiny, flattened animals lack symmetry, mouth, gut, nervous system, and extra-cellular matrix and constitute the apparently monotypic phylum Placozoa. Placozoans diverged early in metazoan history [2–7], making them important organisms for evolutionary research [2,3,8]. Placozoans can be found in warm, shallow, marine environments around the world [9] and all observed individuals fit the general morphological description of T. adhaerens. Our analyses, however, show that the phylum Placozoa is significantly more diverse than previously thought. Extensive genetic variation in Placozoa is revealed (Figures 1 and 2) by four molecular markers: the small and large ribosomal subunits (SSU and LSU), the internal transcribed spacers 1 and 2 and ribosomal 5.8S (ITS), and the large subunit of the mitochondrial ribosome (16S). With SSU, for example, the genetic distances between individual placozoans are comparable to those documented between genera (within families) and even between families (within orders) of other diploblastic, early diverging metazoan phyla (Supplemental Data). Moreover, from only 31 placozoans sampled around the world (Table 1), we obtained eight different haplotypes of mitochondrial 16S (Figure 2), displaying length variation of up to 145 bp, a level far exceeding that documented for any metazoan species or genus. The inferred secondary structures for 16S are correspondingly diverse (Figure 2). Tree topologies inferred from all four markers are largely congruent (Figures 1 and 2). Intra-individual variation in ITS is low relative to the divergences between the five deeper divisions indicated by both 16S and ITS (Figure 2). These data strongly reject the idea that the phylum Placozoa is represented by a single extant species. Thus, caution is warranted in interpreting comparative studies that use a single clonal lineage. In addition, the combined SSU and LSU data (Figure 1), as well as two other recent studies [7,10], convincingly refute the view of placozoans as degenerate medusozoan cnidarians [11]. We have advanced in our understanding of placozoan biodiversity, but much further investigation of these intriguing animals is needed. The species richness of Placozoa is still to be determined. More importantly, placozoans have been studied mostly in the laboratory and nearly all observations have been made on a single clonal lineage, the Grell culture-strain originating from the Red Sea (H1). The importance of studying animals living in their natural habitat is undeniable: a complete reproductive cycle has never been reported in all the decades placozoans have been kept in the laboratory. Based on limited sampling to date, H6, 7 and 8 are exclusively Pacific, and H1, 2, 3 and 5 are not found in the Pacific (Table 1). Otherwise, our data have so far displayed little biogeographic signal. Several placozoan lineages show a widespread and overlapping geographic distribution while several locales have yielded multiple sympatric lineages. A general correlation between small body size and high abundance suggests that microbial eukaryotes (< 1 mm) may be less likely to exhibit biogeographic patterns because their large populations experience few dispersal barriers [12]. When captured in the field on settling