View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Dispatch R1003 Dispatches Animal Evolution: Trichoplax, Trees, and Taxonomic Turmoil The genome sequence of Trichoplax adhaerens, the founding member of the into the same major classes (C, E/F enigmatic animal phylum Placozoa, has revealed that a surprising level of and B) as do those described from genetic complexity underlies its extremely simple body plan, indicating either Amphimedon [4]. Consistent with that placozoans are secondarily simple or that there is an undiscovered a more derived position, however, morphologically complex life stage. Trichoplax has a number of Antp superclass Hox genes that are absent David J. Miller1 and Eldon E. Ball2 but no other axial differentiation, from the sponge Amphimedon. resembling an amoeba. Grell [3] who These include the ‘ParaHox’ gene With the recent or imminent release formally described these common but Trox-2 [5] and the extended Hox of the whole genome sequences of inconspicuous marine organisms as family gene Not [6] known from a number of key animal species, this belonging to a new phylum, assumed previous work. Particularly intriguing is an exciting time for the ‘evo-devo’ that their simplicity is primary, and is the discovery in Trichoplax of many community. In the last twelve months, that they therefore must represent genes associated with neuroendocrine whole genome analyses of the a key stage in animal evolution. This function across the Bilateria; in cnidarian Nematostella vectensis, view is still held by several prominent common with Amphimedon [7], many the choanoflagellate Monosiga Trichoplax biologists, but has always elements of the post-synaptic scaffold brevicollis and the cephalochordate been contentious; the view that it is are present, but so too are channel Branchiostoma floridae (commonly derived from a more complex ancestor and receptor proteins not known from known as amphioxus) have been has recently been gaining momentum sponges. published, each providing significant and is favoured by Srivastava et al. [1]. new perspectives on animal evolution. However, the Trichoplax-basal Are We Missing Something? The whole genome sequence of the scenario cannot be firmly rejected Much of the Trichoplax life cycle is enigmatic placozoan Trichoplax based on their analyses. still unknown. The established means adhaerens was published recently [1] of reproduction are fission, usually in and several other important genomes General Properties of the Trichoplax half, and production of ‘swarmers’ are presently being analysed. The Genome during which up to hundreds of small next few months should see release At around 98 Mb, the Trichoplax fragments, are simultaneously budded of the first whole genome sequence genome is amongst the smallest known off. Molecular markers from a small from a sponge (Amphimedon from any animal; but although the wild-caught population indicate the queenslandica), as well as those of total number of protein-coding genes existence of sexual reproduction [8], several representatives of the second is not large (approximately 11,500), it yet there is no reliable evidence of major protostome lineage, the contains many genes whose homologs sex in the presently known life form. To Lophotrochozoa. When these key have conserved roles in complex quote Pearse and Voight [9] ‘‘not only genomes are available for comparison, patterning processes in ‘higher’ do gametogenesis, embryogenesis, the placozoan data can perhaps be animals (Bilateria). Components of and metamorphosis remain more unequivocally interpreted, but most of the animal-specific and undescribed, but also meiosis, what is most striking about this work developmentally-regulated signalling sperm, and fertilization’’. is that the whole genome sequence pathways are present. Although the If there is indeed a missing life has not definitively resolved the Hedgehog pathway appears to be stage then it may hold the key to the interrelated questions of where absent, as in the sponge, complete genomic complexity reported by Trichoplax fits in animal evolution and Wnt and TGFb pathways are present. Srivastava et al. [1]. So, what is this whether its morphological simplicity is Additionally, the Trichoplax genome missing life stage and where is it ancestral or derived. enocodes most, though not all, Notch hiding? If Pearce and Voight [9] are Churchill could have been thinking and JAK/STAT pathway components, correct and the sexually reproducing of Trichoplax when he said ‘‘It is the apparently missing parts being a life stage is missing, then this implies a riddle, wrapped in a mystery, inside canonical Notch ligand and a Janus that that the eggs and embryos that an enigma’’. The history of placozoan kinase. have repeatedly been reported [1] research has been told several Most of the animal-specific must be something else, perhaps times [2]. Trichoplax is the simplest transcription factors — members of a survival phase analogous to a sponge known animal in terms of cell-type the Sox, Pax, T-box, Fox and Ets gemmule. But if that is the case why diversity — just four types have been families — are represented at a similar do these structures always degenerate described — and structure — it level of complexity to that found in and die? This is just one of the many comprises a flat bilayer of cells with the sponge. For example, the six mysteries that help Trichoplax to distinct upper and lower surfaces, Trichoplax Sox genes appear to fall maintain its enigmatic status. Current Biology Vol 18 No 21 R1004 The Mitochondrial Genome Sometimes Tells a Different Story Whereas the presence of specific genes such as Trox-2 and molecular phylogenetics based on large numbers of nuclear genes [1] imply that the simplicity of Trichoplax is likely to be secondary, features of its Ctenophora Porifera Placozoa Cnidaria Bilateria mitochondrial genome suggest otherwise [14]. Three additional Axial placozoan mitochondrial genomes symmetry CNS; from divergent clades have now been germ/soma sequenced [15]. Whilst all four of these Nervous system, segregation placozoan mitochondrial genomes muscle cells Hox-like contain the ‘normal’ animal gene genes complement (although they all appear to lack atp8), they resemble Monosiga and other non-metazoans in two respects — they are all much larger (32–43 kb) than the vast majority of bilaterian mitochondrial genomes, and Multicellularity : axial patterning via Wnt, TGF β : nervous they also contain a number (three in the Urmetazoa system : muscle : stem and germ cells : Antp superclass case of T. adhaerens) of large open and other metazoan-specific genes reading frames of unknown function. Viewed in isolation, these Current Biology characteristics would seem to point to placozoans as the basal metazoans. Figure 1. Possible evolutionary relationships at the base of the Metazoa. However, a recent Bayesian analysis, Whilst the Ctenophora are morphologically complex, a recent large-scale phylogenomic anal- based on 13 protein sequences ysis [12] places them at the base of the Metazoa, implying that the morphological simplicity of encoded by most mitochondrial both sponges and placozoans is derived. The Dunn et al. [12] study did not include Placozoa; genomes, found that placozoans are the whole genome sequence analysis [1] and qualitative aspects of its nuclear genome, includ- a sister group to the Bilateria [16]. ing the presence of members of the extended Hox gene family, support the position shown It is most unfortunate that none of here. However, the mitochondrial genomes of Placozoa are more ‘primitive’ in structural terms than would be expected under this scenario. Green bars and associated text indicate gains, the recent large-scale studies have and red bars and text losses during evolution. included all of the lower metazoan phyla. Thus, Dunn et al. [12] did not Lower Metazoan Relationships phylogenomic analysis [12], support include Placozoa and Srivastava Whilst the Bilateria is a well-defined a very different view of lower animal et al. [1] did not include Ctenophora. phylogenetic group, both the relationships (Figure 1), with It would be particularly interesting to branching order of the ‘lower’ animal ctenophores as the basal animal see the dataset run by Dunn et al. [12] phyla — Porifera, Placozoa, Cnidaria group, implying that both sponges and rerun with the inclusion of the and Ctenophora — and their placozoans are secondarily simple. appropriate placozoan genes. relationships to the Bilateria remain Although it is true that the contentious. Their branching order is ctenophores are not yet well Degeneration from a Complex often assumed to be reflected in their represented in the sequence State — Is There a Pattern? relative morphological complexity, databases, there are no obvious Traditionally it has been assumed that, which increases from Placozoa, molecular criteria that contradict this with the exception of a few aberrant through Porifera and Cnidaria, with view; for example, as in the case of organisms such as Trichoplax, extant the Ctenophora branching immediately sponges (but unlike cnidarians), levels of morphological complexity below the Bilateria (for example [10]). ctenophores appear to lack Hox-like represent progressive steps in animal Some aspects of this scheme hold up: and ‘ParaHox’ genes [13]. Although evolution — essentially, that what the Cnidaria are unquestionably more lacking Hox-like genes, Trichoplax we see now is as ‘advanced’ as complex, in