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Animal : , Trees, and Taxonomic Turmoil

The sequence of Trichoplax adhaerens, the founding member of the into the same classes (C, E/F enigmatic , has revealed that a surprising level of and B) as do those described from genetic complexity underlies its extremely simple , indicating either [4]. Consistent with that placozoans are secondarily simple or that there is an undiscovered a more derived position, however, morphologically complex stage. Trichoplax has a number of Antp superclass Hox that are absent David J. Miller1 and Eldon E. Ball2 but no other axial differentiation, from the Amphimedon. resembling an . Grell [3] who These include the ‘ParaHox’ With the recent or imminent release formally described these common but -2 [5] and the extended Hox of the whole genome sequences of inconspicuous marine as gene Not [6] known from a number of key animal , belonging to a new phylum, assumed previous work. Particularly intriguing is an exciting 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 ; in cnidarian vectensis, view is still held by several prominent common with Amphimedon [7], many the choanoflagellate Monosiga Trichoplax , but has always elements of the post-synaptic scaffold brevicollis and the been contentious; the view that it is are present, but so too are channel floridae (commonly derived from a more complex ancestor and receptor not known from known as amphioxus) have been has recently been gaining momentum . published, each providing significant and is favoured by Srivastava et al. [1]. new perspectives on animal evolution. However, the Trichoplax- 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 are fission, usually in and several other important 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 -coding genes existence of [8], several representatives of the second is not large (approximately 11,500), it yet there is no reliable evidence of major lineage, the contains many genes whose homologs in the presently known life form. To . 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 can perhaps be (Bilateria). Components of and remain more unequivocally interpreted, but most of the animal-specific and undescribed, but also , what is most striking about this work developmentally-regulated signalling , 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 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 that that the and 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 [2]. Trichoplax is the simplest factors — members of a survival phase analogous to a sponge known animal in terms of -type the Sox, , T-box, 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 based on large numbers of nuclear genes [1] imply that the simplicity of Trichoplax is likely to be secondary, features of its Porifera Placozoa Bilateria mitochondrial genome suggest otherwise [14]. Three additional Axial placozoan mitochondrial genomes CNS; from divergent have now been germ/soma sequenced [15]. Whilst all four of these , 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- 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 to the Bilateria [16]. ing the presence of members of the extended 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 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 having many metazoan- has a ‘ParaHox’ gene — Trox-2 [5] is a particular lineage ever got. Other specific gene families, than are either clearly related to the cnox2 genes of interpretations have always existed, Placozoa or Porifera. For example, cnidarians, Ind and the however, and, intriguingly, a number whereas Nematostella has members of Gsx genes. Both the of recent large-scale studies have most or all of the 12 Wnt subfamilies presence of this gene and its breathed life into the old that loss [11], very few Wnts are encoded by the expression pattern are consistent with of morphological complexity may be Amphimedon or Trichoplax genomes. a derived position for placozoans as a common theme in animal evolution. Whilst placozoans and sponges are shown in Figure 1; homologs of Trox-2 The consensus ‘new view’ of unquestionably less morphologically have roles in the nervous system from evolution (for example [17]) complex than cnidarians and Cnidaria to , and its has as the sister group to the ctenophores, several lines of evidence, expression in marginal cells suggests , and the cephalochordate including a recent large-scale a possible sensory role [5]. amphioxus as representative of the Dispatch R1005 basal chordate lineage. As discussed fit — more sequence data from 11. Kusserow, A., Pang, K., Sturm, C., Hrouda, M., Lentfer, J., Schmidt, H.A., Technau, U., von above, there is now substantial ctenophores are urgently required. Haeseler, A., Hobmayer, B., Martindale, M.Q., molecular support for the idea that Other outstanding questions include et al. (2005). Unexpected complexity of the ctenophores branch most basally how placozoans have maintained Wnt gene family in a . 433, 156–160. within the animal , implying large and complex mitochondrial 12. Dunn, C.W., Hejnol, A., , D.Q., Pang, K., that sponges are secondarily simple. genomes, and whether sponges are Browne, W.E., Smith, S.A., Seaver, E., Rouse, G.W., Obst, M., Edgecombe, G.D., et al. The case for a morphologically monophyletic or paraphyletic. (2008). Broad phylogenomic sampling improves complex common bilaterian ancestor Although sponges are classically resolution of the animal . Nature 452, (Urbilateria) has been eloquently lumped together, there is an emerging 745–749. 13. Pang, K., and Martindale, M.Q. (2008). made by de Robertis [18] and others, view that the phylum Porifera is a Developmental expression of genes but these recent large-scale studies paraphyletic group, homoscleromorph in the ctenophore leidyi. Dev. Genes Evol. 218, 307–319. imply that this also holds for Urmetazoa sponges (such as Oscarella) being 14. Dellaporta, S.L., Xu, A., Sagasser, S., and Urchordata. Hence, not only is most closely related to the . Jakob, W., , M.A., Buss, L.W., and genetic complexity ancestral [19,20], We live in interesting times indeed. Schierwater, B. (2006). Mitochondrial genome of Trichoplax adhaerens supports placozoa as but the same may be true for the basal lower metazoan phylum. Proc. Natl. morphological complexity as well. References Acad. Sci. USA 103, 8751–8756. 1. Srivastava, M., Begovic, E., Chapman, J., 15. Signorovitch, A.Y., Buss, L.W., and Putnam, N.H., Hellsten, U., Kawashima, T., Dellaporta, S.L. (2007). Comparative genomics Outstanding Questions Kuo, A., Mitros, T., Salamov, A., of large mitochondria in placozoans. PLoS As outlined above, these are interesting Carpenter, M.L., et al. (2008). The Trichoplax . 3, e13. genome and the nature of placozoans. Nature 16. Ruiz-Trillo, I., Roger, A.J., Burger, G., times for students of evolutionary 454, 955–960. Gray, M.W., and Lang, B.F. (2008). A genomics, with genome sequencing 2. , D.J., and Ball, E.E. (2005). Animal phylogenomic investigation into the origin of in progress for representatives of evolution: the enigmatic phylum placozoa metazoa. Mol. Biol. Evol. 25, 664–672. revisited. Curr. Biol. 15, R26–R28. 17. Delsuc, F., Brinkmann, H., Chourrout, D., and several missing key phyla. It is to be 3. Grell, K.G. (1971). Trichoplax adhaerens F.E. Philippe, H. (2006). Tunicates and not hoped that decreasing costs Schulze und die Entstehung der Metazoen. are the closest living Naturwiss. Rundschau 24, 160–161. relatives of vertebrates. Nature 439, 965–968. the determination of whole genome 4. Larroux, C., Luke, G.N., Koopman, P., 18. De Robertis, E.M. (2008). Evo-Devo: Variations sequences for more representatives Rokhsar, D.S., Shimeld, S.M., and on ancestral themes. Cell 132, 185–195. of each phylum in the near future, as Degnan, B.M. (2008). Genesis and expansion 19. Technau, U., Rudd, S., Maxwell, P.,Gordon, P.M., of metazoan gene classes. Saina, M., Grasso, L.C., Hayward, D.C., gene losses in individual lineages Mol. Biol. Evol. 25, 980–996. Sensen, C.W., Saint, R., Holstein, T.W., et al. obscure general patterns, and many 5. Jakob, W., Sagasser, S., Dellaporta, S., (2005). Maintenance of ancestral complexity and Holland, P., Kuhn, K., and Schierwater, B. non-metazoan genes in two basal cnidarians. animal phyla are very diverse. (2004). The Trox-2 Hox/ParaHox gene of Trends Genet. 21, 633–639. With so much sequence data now Trichoplax (Placozoa) marks an epithelial 20. Putnam, N.H., Srivastava, M., Hellsten, U., available for Trichoplax, it will be boundary. Dev. Genes Evol. 214, 170–175. Dirks, B., Chapman, J., Salamov, A., Terry, A., 6. Martinelli, C., and Spring, J. (2004). Expression Shapiro, H., Lindquist, E., Kapitonov, V.V., et al. fascinating to see where and when pattern of the homeobox gene Not in the basal (2007). Sea anemone genome reveals ancestral the homologs of many of the key metazoan Trichoplax adhaerens. Gene Exp. eumetazoan gene repertoire and genomic Patterns 4, 443–447. organization. Science 317, 86–94. development regulators are expressed. 7. Sakarya, O., Armstrong, K.A., Adamska, M., Very few expression patterns are yet Adamski, M., Wang, I.F., Tidor, B., 1ARC Centre of Excellence for available, but these imply much greater Degnan, B.M., Oakley, T.H., and Kosik, K.S. (2007). A post-synaptic scaffold at the origin Studies, James Cook University, Townsville, cell diversity than does morphology of the animal kingdom. PLoS ONE 2, e506. Queensland 4811, Australia. 2ARC Centre for alone. It is possible, however, that 8. Signorovitch, A.Y., Dellaporta, S.L., and the Molecular of Development, many of these genes are not expressed Buss, L.W. (2005). Molecular signatures for sex Research School of Biological Sciences, in the Placozoa. Proc. Natl. Acad. Sci. USA 102, Australian National University, Canberra, in the presently known life form. 15518–15522. ACT 2600, Australia. Notwithstanding the importance of the 9. Pearse, V.B., and Voigt, O. (2007). biology of placozoans (Trichoplax): distribution, E-mail: [email protected], eldon.ball@ forthcoming whole genome sequence diversity, biotic interactions. Int. Comp. Biol. .edu.au for the sponge Amphimedon, the 47, 677–692. 10. Nielsen, C. (2008). Six major steps in animal most intriguing question of all at evolution: are we derived sponge larvae? Evol. the moment is where the ctenophores Dev. 10, 241–257. DOI: 10.1016/j.cub.2008.09.016

Visual : Retinotopy parts of the visual field. This ‘topographic’ relationship maintains a Meets Percept-otopy? systematic structure on a large scale, so that each half of the visual field is mapped onto the contralateral In the mammalian , the primary visual cortex forms a systematic spatial hemisphere [1]. Figure 1 shows that, of the visual field. A new study suggests that the representations on this when a observer views a map are affected by visual illusions that alter perceived size. Spatial patterns high-contrast checkerboard ring, of activity may thus reflect perceived size. a corresponding ring-like swath of activity is generated upon the cortical Alexander C. Huk in visual neuroscience. In the early surface. This isomorphic relationship visual cortices of many animals is typically assumed to be inherited: Retinotopic organization is a (including monkeys and ), so long as the wiring that connects fundamental organizational element nearby respond to adjacent the to the cortex is not