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and 66 (2013) 551–557

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Molecular Phylogenetics and Evolution

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Review Chasing the urmetazoon: Striking a blow for quality data? ⇑ Hans-Jürgen Osigus a, Michael Eitel a,d, Bernd Schierwater a,b,c, a ITZ, Division of and Evolution, Stiftung Tieraerztliche Hochschule Hannover, Germany b American Museum of Natural History, New York, USA c Department of Ecology and Evolutionary , Yale University, USA d The Swire Institute of Marine Science, Faculty of Science, School of Biological Sciences, The University of Hong Kong, Hong Kong article info abstract

Article history: The ever-lingering question: ‘‘What did the urmetazoan look like?’’ has not lost its charm, appeal or elu- Available online 6 June 2012 siveness for one and a half centuries. A solid amount of organismal data give what some feel is a clear answer (e.g. Placozoa are at the base of the metazoan tree of (ToL)), but a diversity of modern molec- Keywords: ular data gives almost as many answers as there are exemplars, and even the largest molecular data sets Urmetazoon could not solve the question and sometimes even suggest obvious zoological nonsense. Since the prob- Trichoplax lems involved in this phylogenetic conundrum encompass a wide array of analytical freedom and uncer- Placozoa tainty it seems questionable whether a further increase in molecular data (quantity) can solve this Non-bilaterian animals classical deep phylogeny problem. This review thus strikes a blow for evaluating quality data (including Placula hypothesis Metazoan evolution morphological, molecule morphologies, arrangement, and gene loss versus gene gain data) in an appropriate manner. Ó 2012 Elsevier Inc. All rights reserved.

Contents

1. Traditional morphological views ...... 551 2. Modern molecular views ...... 552 2.1. Analyzing gene sequences (so-called ‘‘quantity data’’) ...... 552 2.2. Analyzing gene presence and structure (so-called ‘‘quality data’’)...... 553 2.2.1. Hox-/ParaHox ...... 553 2.2.2. Pax genes ...... 554 2.2.3. Dicer genes ...... 554 2.2.4. Leucine-rich repeat containing G protein-coupled receptors (LGRs)...... 554 2.2.5. Ribosomal genes ...... 554 2.2.6. Mitochondrial genome characteristics ...... 554 3. Summary quantity versus quality data...... 555 Acknowledgments ...... 555 References ...... 556

1. Traditional morphological views ple , perhaps just complex enough to pass the bridge between a and a metazoan. This bridge is the possession Three prominent urmetazoan hypotheses are most often under of more than one somatic cell type ( may consist of doz- debate, (i) the placula, (ii) the planula and (iii) the gastrea ens or hundreds of cells and may have more than one cell type hypothesis (Bütschli, 1884; Haeckel, 1874; Lankester, 1877, for within a colony but they never have two or more different so- overview see Kaestner, 1980). Common to all hypotheses is that matic cells). Intrasomatic differentiation, which is the invention the hypothetical ‘‘urmetazoon’’ must have had an extremely sim- of the urmetazoon and a synapomorphy for all metazoans, became the motor for radiation of the metazoan bauplans (cf. Boero et al., 2007; Schierwater, B., de Jong, D., Desalle, R., 2009). ⇑ Corresponding author at: Division of Ecology and Evolution, Stiftung Tieraerz- Unfortunately for phylogenetics at the base of the tree, however, tliche Hochschule Hannover, Bünteweg 17d, D-30559 Hannover, Germany. Fax: +49 morphology was ‘‘frozen’’ as very subtle and uninterpretable 511 953 8485. E-mail address: [email protected] (B. Schierwater). anatomical changes occurred, and hence we are left with very

1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.05.028 552 H.-J. Osigus et al. / Molecular Phylogenetics and Evolution 66 (2013) 551–557 few anatomical characters. In sharp contrast, the more derived choanocytes, and not vice versa (Clark, 1868; Kent, 1878; Maldo- root of the tree invented a third germ layer, the mesoderm, which nado, 2004). In sum, there are currently two reasonable candidates fueled an explosion of bauplan radiation and new anatomical for the closest living relative of the urmetazoon, Placozoa and characters in the Bilateria. Porifera. Placozoans meet the expectations of a primitive but general urmetazoan bauplan (see Fig. 1); they possess the simplest bau- plan among extant metazoans (Grell and Benwitz, 1971; Grell 2. Modern molecular views and Ruthmann, 1991; Schierwater, 2005; Schulze, 1883, 1891). Only five somatic cell types (Guidi et al., 2011; Jakob et al., 2.1. Analyzing gene sequences (so-called ‘‘quantity data’’) 2004) have been recognized. The simplicity of placozoans is fur- ther highlighted by their lack of any kind of axis of symmetry, or- Early molecular systematic studies used single gene data sets gans, nerve and muscle cells, lamina, and an ultrastructurally (mainly 18S or 28S rRNA) to resolve conflicts at the base of the identifiable extracellular matrix (note however, several cell–cell metazoan . The resulting mixture of trees mostly sup- contact genes have been identified in Trichoplax; Chapman et al., ports the traditional view of early branching Porifera (for overview 2010). In contrast to placozoans, Porifera usually possess more see Schierwater et al., 2010a), sometimes with the Placo- than a dozen somatic cell types (see Jiang and Xu, 2010; Valentine zoa jumping inside a of (Bridge et al., 1995; Siddall et al., 1994, for an overview of cell types in animals) and normally et al., 1995). Analysis of mitochondrial protein coding sequence also develop an extracellular matrix (ECM) and basal membrane data have promised to lead to a more reasonable picture of early (e.g. Boury-Esnault et al., 2003) or even complete sealing epithelia animal evolution supporting a split between Bilateria and (Adams et al., 2010). In Cnidaria and Ctenophora morphological non-bilaterian animals with Placozoa branching first within the complexity has increased. Thus many zoologists have been consid- non-Bilateria (Dellaporta et al., 2006; Signorovitch et al., 2007). ering Placozoa as the closest living relative to the urmetazoon (e.g. Nevertheless, analyses of recently sequenced mitochondrial gen- Grell, 1971, 1982; Schulze, 1891). A larger group of researchers has omes from Ctenophora (Kohn et al., 2012; Pett et al., 2011) seen the sponges, Porifera, closest to the base of the metazoan tree highlight limitations of analyses based on mitochondrial protein of life. The main argument here has been a single-character argu- sequence data. One of several problems relates to the observation ment, the possession of the -catching character choanocytes, that mitochondrial sequences in Ctenophora have evolved several i.e. the morphological similarity between the choanocytes in the times faster than in other animal phyla. sponge gastrodermis and the single-celled choanoflagellates. But The rapid progress in next generation sequencing techniques there also are other explanations for this observation than a and computational data processing opens the door for phyloge- non-simple evolutionary transformation of a choanoflagellate col- netic analyses using large whole genome and EST data sets includ- ony into a sponge bauplan. Some authors are in favor of a conver- ing several hundred or thousands of genes. As a consequence gent evolution of collar structures and metazoan choanocytes phylogenomic approaches to elucidate adaptive evolution in genes (Maldonado, 2004) or even claim that the choanoflagellates are de- and genomes will become an important field in future research (cf. rived sponges. For example, several genes in the choanoflagellate Goodman and Sterner, 2010; Shinzato et al., 2011). At present we genome (including genes for metazoan style cell adhesion and cell are mostly limited to non-causal analyses of descriptive characters, signaling; King et al., 2003; Manning et al., 2008) might be seen like gene sequences. At the base of the metazoan ToL, the outcome as indicators that evolution here went the opposite of the of such analyses has been highly contradictory and can be summa- obvious way, i.e. that choanoflagellates originated from sponge rized in three main scenarios:

Fig. 1. (A) Photograph of Trichoplax adhaerens, Schulze (1883). For additional images of placozoan specimens see www.trichoplax.com. (B) Modern placula hypothesis of metazoan origin (for details see Schierwater et al., 2009a). (from Schierwater et al., 2009a). H.-J. Osigus et al. / Molecular Phylogenetics and Evolution 66 (2013) 551–557 553

Fig. 2. Deep metazoan relationships (A) The traditional view sees the Porifera in a basal position of the metazoan tree of life with Placozoa deriving next and Cnidaria and Ctenophora forming the Coelenterata. (B) The alternative traditional view sees Placozoa basal and in this case the Porifera deriving next. (C) A modified view of the traditional scenario in (B) supports a relationship between Bilateria and non-bilaterian animals with Placozoa branching first within the non-Bilateria. (D) One of the surprising topologies that derive from certain molecular analyses which put the morphologically derived Ctenophora in a basal position.

(i) The traditional ‘‘Porifera first scenario’’ is supported by some sampling, misidentified taxa, the inclusion of non-orthologous or recent molecular studies by, e.g. Philippe et al. (2009), saturated genes, chimeric sequences or an inappropriate evolu- Fig. 2A). Despite of the large data sets and the optimized tionary model can lead to artifacts and well phylogenetic analyses several important nodes and espe- supported which are in conflict with zoological knowledge cially the position of Placozoa are not well supported in (Philippe et al., 2011). these phylogenetic inferences and some studies even doubt the of sponges (e.g. Sperling et al., 2009). How- 2.2. Analyzing gene presence and structure (so-called ‘‘quality data’’) ever, recent studies, e.g. on the evolution of post-synaptic proteins (Alie and Manuel, 2010) use a ‘‘Placozoa basal’’ sce- There are several approaches to infer evolutionary relationships nario (Fig. 2B) to reconstruct the most parsimonious way of based on the presence or absence or genomic organization of genes evolution of these proteins in Metazoa. of a distinct gene . We just list a few examples. (ii) A second scenario has been suggested in a study combining morphological and molecular data (from both nuclear and 2.2.1. Hox-/ParaHox genes mitochondrial genes) in one concatenated data matrix Hox-/ParaHox genes play important roles in pattern formation (Schierwater et al., 2009a, Fig. 2C). This study postulates along the anterior-posterior axis in bilaterian animals (Carroll, the monophyly of the Porifera but places them in a more 1995). Both the inventory and the structure of Hox-/ParaHox-like derived position within the diploblasts with Placozoa as genes suggest an early diploblast-bilateria split and provides evi- the earliest branching diploblast phylum and Cnidaria and dence for the placozoan Trox-2 gene being the Proto-Hox/Parahox Ctenophora forming a ‘‘Coelenterata’’ (Leuckart, gene for all metazoans (Jakob et al., 2004). Since sponges and cte- 1848). The most remarkable point, however, is the sister nophores probably do not possess any Hox genes, the above sce- group relationship of the monophyletic Bilateria and the nario assumes a loss of Hox-/ParaHox-like genes in both phyla monophyletic non-bilaterians (i.e. Placozoa, Porifera, (for literature and controversial views see Chourrout et al., 2006; Cnidaria and Ctenophora) with high support values. A subse- Garcia-Fernandez, 2005; Ryan et al., 2007; Schierwater and Kamm, quent study with increased sampling (Schierwater 2010). Based on the presence of Hox/Parahox genes the so-called et al., 2009b) as well as mitochondrial sequence data (Della- taxon ‘‘ParaHoxozoa’’ was suggested, which includes Placozoa, Cni- porta et al., 2006) gave further support for this scenario. daria and Bilateria (Ryan et al., 2010) and unifies two distantly re- (iii) A third scenario with the morphologically complex Cte- lated animal phyla, the Porifera and Ctenophora, as a sister group nophora as the earliest branching metazoan phylum has to this so-called ‘‘subkingdom’’. If ‘‘ParaHoxozoa’’ are meant as a been suggested based on molecular data only (Dunn et al., natural rather than an artificial clade, this scenario must be seen 2008; Hejnol et al., 2009, Fig. 2D). With special regard to with great caution, however. Besides the zoological problem of the base of the metazoan tree of life the latter, hot debated uniting two distinct phyla without any clade diagnostic morpho- scenario not only suggested Ctenophora as sister group to logical or developmental synapomorphy, the loss of a single gene all other animals but also placed Placozoa between the Dem- (Proto Hox/ParaHox gene) is not a very strong character. If one ospongiae and Homoscleromorpha supporting of wants to assume that neither Porifera nor Ctenophora ever pos- sponges. A most recent analysis shows that the positioning sessed a Hox like gene and that they form a monophyletic group, of the highly derived Ctenophora is likely the result of a long this would put a highly derived animal group (Ctenophora) to- branch attraction (LBA) artifact (Nosenko et al., unpublished gether with one of the basal groups (Porifera) and would create data). sharp conflicts to our knowledge from comparative . Some people may also argue that gene information from a yet incom- Several studies (e.g. Philippe et al., 2011; Pick et al., 2010) have plete genome of a single may not necessarily be represen- re-analyzed the previously mentioned data sets and list several key tative for the phylum. Thus, the question whether Hox-like genes factors, which strongly influence the outcome of the analyses. It are indeed absent in Porifera and Ctenophora remains open. If ab- has been shown that the choice of outgroups, the ingroup taxon sent, the question whether this is an ancestral or derived feature 554 H.-J. Osigus et al. / Molecular Phylogenetics and Evolution 66 (2013) 551–557

Fig. 3. Pax gene evolution model. Based on the structural features of Pax genes, i.e. paired (s), homeodomain and octapeptide, an evolutionary scenario has been suggested in which a PaxB-like Ur-Pax gene is the starting point for several duplication events that led to a large diversity of Pax gene subfamilies in Cnidaria and Bilateria (for details see Hadrys et al., 2005). Paired domains (PD) = green rectangles, homeodomains (HD) = black rectangles, octapeptides (OP) = blue circles. (from Hadrys et al., 2005). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

remains open, too. According to current knowledge placozoans the bursicon receptor in (cuticle hardening) (Van Loy et al., possess the most ancient Hox-/ParaHox system in the Metazoa. 2008). Based on phylogenetic inferences and structural data it has been proposed that placozoan LGRs may represent an ancient form 2.2.2. Pax genes of metazoan LGRs (Van Hiel et al., 2011). Comparative data from The Pax gene family consists of tissue specific transcription fac- sponges and ctenophores are missing yet. tors that are important in early animal development for the spec- ification of tissues and organs (Chi and Epstein, 2002). The 2.2.5. Ribosomal genes structure of Pax genes (i.e. the partial or complete presence of Ribosomal genes show a tendency for size reduction from pro- homeo- and paired domains and octapeptide motifs) suggests that tists to higher metazoans. An illustrative example is shown in En- a putative Proto-Pax gene was similar to the PaxB gene found in der and Schierwater (2003), where placozoans possess the longest Trichoplax (Hadrys et al., 2005; Fig. 3). Sponges also possess a single and most complex 16S rRNA morphology. Both size and complex- PaxB gene. Pax genes from Ctenophora have not been described ity get gradually reduced from Placozoa to Porifera to Cnidaria and yet. The Cnidaria and Bilateria show a large radiation of Pax genes finally Bilateria. Ctenophores show by far the most reduced 16S (Hill et al., 2010). Thus, the sum of available evidence is congruent rRNA genes of all basal metazoans (Pett et al., 2011; Kohn et al., with the hypothesis that the placozoan Pax gene is ancestral to the 2012). Again, The parsimonious interpretation of the observed Pax genes in other phyla, but the data set may be incomplete yet. molecule morphology data is that placozoans mirror the most ancestral condition within extant metazoans. 2.2.3. Dicer genes Proteins of this gene family are essential components of the 2.2.6. Mitochondrial genome characteristics RNA interference pathway (for review see McManus, 2004). A re- With respect to gene presence/absence and gene arrangement cent study (de Jong et al., 2009) has shown that the Placozoa is data mitochondrial (mt) genomes provide a rich repertoire of phy- the only known metazoan phylum which contains both represen- logenetically informative characters at different taxonomic levels. tatives of an ancient duplication event. Like all other metazoan ani- It is believed that one of the strongest characters for phylogenetic mals, sponges only possess group II dicer proteins. These data are reconstruction is gene loss. The latter occurs regularly, but the re- consistent with the hypothesis that only the Placozoa still harbor verse, i.e. regaining and incorporating a formerly lost gene into a the direct descendents of a ‘Proto-Dicer’ gene. mitochondrial genome, must be an extremely rare event. If several genes need to be regained and incorporated the likelihood for such 2.2.4. Leucine-rich repeat containing G protein-coupled receptors an event jumps beyond probability values generally accepted in (LGRs) biology. The placozoan mt genomes represent the most complete LGRs are seven-transmembrane domain receptors with impor- mt genomes among metazoans and according to the phylogenetic tant functions in development and reproduction. They include such interpretation of gene loss data the placozoan mitochondrial prominent proteins as the relaxin receptors in , as well as genomes would represent the most ancestral condition found in H.-J. Osigus et al. / Molecular Phylogenetics and Evolution 66 (2013) 551–557 555

Fig. 4. Overall tendencies in early metazoan mitochondrial genome evolution. Mitochondrial genome evolution from Protozoa (represented by Choanoflagellata) to early metazoan phyla (Placozoa, Porifera, Cnidaria and Ctenophora). A clear tendency to genome compaction is visible (see text). A special case of mt genome evolution has been described in Cnidaria, where ancestrally circular become linearized or even linear fragmented in more derived cnidarian taxa. metazoans. For example, the number of open reading frames tRNAs especially Cnidaria or Ctenophora tend to reduce the num- (ORFs) in Placozoa is up to eight (Dellaporta et al., 2006; Signorov- ber of encoded tRNA genes within non-bilaterian animals down itch et al., 2007), while sponges and cnidarians only exceptionally to one tRNA. In Porifera the number of tRNA ranges from some 2 harbor up to three. In metazoan outgroups the number of ORFs is to 27, mirroring both secondary reduction and duplication events. usually high, e.g. in the choanoflagellate Monosiga brevicollis we Summarizing all of the mitochondrial jigsaw pieces the placozo- find 6 additional ORFs while the ichthyosporean Amoebidium para- an mt genome shows the highest similarity to protozoan mt gen- siticum harbors at least 24 (Burger et al., 2003). Obviously a high omes and almost looks like an evolutionary link between protists number of ORFs is an ancestral metazoan feature. and metazoan mt genomes. Whether the unequivocal basal mt From protozoans to derived metazoans mitochondrial genomes genome features of the Placozoa also mirror a basal position for show a clear tendency for the reduction of non-coding intergenic the phylum may be seen as a different question. spacer regions and genome size in general (Fig. 4). In protist groups such as Ichthyosporea, Filasterea and Choanoflagellata large mito- 3. Summary quantity versus quality data chondrial genomes around 60 kb or more are the normal case. As several molecular studies support a sister group relationship be- The sum of molecular trees based on large numbers of gene se- tween the Choanoflagellata and metazoans the large mt genome quences does not resolve phylogenetic relationships at the base of of Monosiga brevicollis (76 kb) might be seen as a reference mt gen- the Metazoa. Conflicting scenarios have been published in short se- ome for early metazoans. The largest animal mitochondrial gen- quence and each single analysis can be criticized for one or the omes have been found in placozoans (32–43 kb), the second other reason. It is unclear to many whether the base of Metazoa largest mt genomes in sponges (16–29 kb), and cum grano salis nor- can ever be resolved by means of sequence data even if whole gen- mal sized mitochondrial genomes in almost all other metazoans omes and extensive taxon sampling is used. The opposite data (16–18 kb). An interesting apomorphy is seen in Cnidaria, where type, i.e. the so-called ‘‘quality data’’ in the form of anatomical, the basal Anthozoa harbor circular mt genomes of 15–21 kb size developmental, molecule morphology, gene loss, gene structure whereas the derived Scyphozoa, , Staurozoa and Cubozoa and gene arrangement data is comparatively very limited with re- have linearized and sometimes highly fragmented mitochondrial spect to the number of available characters, but provides less con- genomes (up to eight chromosomes in cubozoans) with a total fusion. The majority of the data support a basal position of the length of up to 28 kb in cubozoans (Smith et al., 2012, for overview Placozoa near the root of the metazoan tree of life. The real prob- see Kayal et al., 2012). The most derived mt genomes are found in lem, however, remains completely unresolved, the problem of the Ctenophora, where the overall mt genome size is only about the relative character weighting between ‘‘quality data’’ on the 11 kb and the number of encoded genes as well as the coding se- one hand and molecular sequence data on the other hand. Solving quence of identified genes is highly reduced (Kohn et al., 2012; Pett this problem is far away from trivial but it must eventually be ad- et al., 2011). dressed in to be able to perform concatenated analyses in a In addition to the presence of additional open reading frames useful way, particularly at the most difficult part of the metazoan and large intergenic regions in the placozoan mitochondrial gen- tree of life, its root. omes, these also harbor several introns as well as a full comple- ment of 24 tRNA genes. Although introns are regularly also found in Porifera and Cnidaria the trans-splicing group I introns in Placo- Acknowledgments zoa seem to be unique to this phylum (Burger et al., 2009). In high- er animal phyla introns or intergenic spacers are rare or absent We thank Rob DeSalle (AMNH, New York) and Stephen Della- features. In Bilateria, but also already seen in Porifera, Cnidaria porta (Yale University) for intellectual input and comments on and Ctenophora, the reduction has progressed to a degree that the manuscript. H.J.O acknowledges a doctoral fellowship from genes are overlapping. With respect to mitochondrial encoded the Studienstiftung des deutschen Volkes. M.E. acknowledges 556 H.-J. Osigus et al. / Molecular Phylogenetics and Evolution 66 (2013) 551–557 funding by the Evangelisches Studienwerk e.V. Villigst, the Stiftung Hadrys, T., DeSalle, R., Sagasser, S., Fischer, N., Schierwater, B., 2005. 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