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A Developmental Perspective: Changes in the Position of the Blastopore during Bilaterian Evolution

2009; Elsevier BV; Volume: 17; Issue: 2 Linguagem: Inglês

10.1016/j.devcel.2009.07.024

1878-1551

Mark Q. Martindale, Andreas Hejnol,

Marine and coastal plant biology

Progress in resolving the phylogenetic relationships among animals and the expansion of molecular developmental studies to a broader variety of organisms has provided important insights into the evolution of developmental programs. These new studies make it possible to reevaluate old hypotheses about the evolution of animal body plans and to elaborate new ones. Here, we review recent studies that shed light on the transition from a radially organized ancestor to the last common ancestor of the Bilateria (“Urbilaterian”) and present an integrative hypothesis about plausible developmental scenarios for the evolution of complex multicellular animals. Progress in resolving the phylogenetic relationships among animals and the expansion of molecular developmental studies to a broader variety of organisms has provided important insights into the evolution of developmental programs. These new studies make it possible to reevaluate old hypotheses about the evolution of animal body plans and to elaborate new ones. Here, we review recent studies that shed light on the transition from a radially organized ancestor to the last common ancestor of the Bilateria (“Urbilaterian”) and present an integrative hypothesis about plausible developmental scenarios for the evolution of complex multicellular animals. Evolutionary developmental biologists have attempted to understand the molecular basis for differences in the organization of animal body plans and to generate plausible, testable scenarios for how these molecular programs could be modified to give rise to novel forms. Most of this work has focused on a monophyletic group of triploblastic animals, the Bilateria: animals that possess an anterior-posterior axis and a dorsoventral axis that define a plane of bilateral symmetry. In addition to derivatives of ectoderm (skin and nervous system) and endoderm (gut and its derivatives), triploblastic animals have derivatives of the third “middle” germ layer called mesoderm, which includes musculature, the circulatory system, excretory system, and the somatic portions of the gonad. Bilaterians have historically been divided into two major evolutionary groups (Figure 1): the deuterostomes (which includes vertebrates like human beings) and the protostomes (which includes the majority of other invertebrate animals, including the developmental model systems C. elegans and Drosophila). These groups were named over 100 years ago and were defined on the basis of embryological principles. Typically in deuterostomes, the position in the embryo that gives rise to endodermal tissues (called the blastopore) at the onset of gastrulation gives rise to the anus of the adult animal. The mouth of deuterostomes (“secondary mouth”) forms at a different location. In the last common ancestor of all protostomes (“mouth first”), the site of gastrulation was said to give rise, not to the anus, but to the adult mouth. These terms are a testament to our recognition of the importance of changing patterns of developmental patterns in the generation of body plan diversity during organismal evolution. Reconstructing molecular and morphological characteristics of the “Urbilaterian” (the last common ancestor of all bilaterians) has been a central goal in evolutionary developmental biology. Fueling this effort is the fact that most of the available information about the cellular and molecular details of development is gleaned from a handful of genetic models systems (Figure 1) such as mice (deuterostomes) and flies and nematodes (protostomes). These systems revealed some shared developmental molecular mechanisms between protostome and deuterostomes, leading to the idea that their last common ancestor was a complex organism with a reiterated, segmented body plan, a central nervous system with an anterior brain, a through gut with a ventral mouth, and a mesodermally derived circulatory system and coelom (body cavity) (see e.g., De Robertis and Sasai, 1996De Robertis E.M. Sasai Y. A common plan for dorsoventral patterning in Bilateria.Nature. 1996; 380: 37-40Crossref PubMed Scopus (568) Google Scholar). However, the most recent phylogenetic arguments that incorporate a much greater spectrum of the existing biological diversity (Figure 1) demonstrate that these morphological features are not likely characteristics of the Urbilaterian (Baguñá and Riutort, 2004Baguñá J. Riutort M. The dawn of bilaterian animals: the case of acoelomorph flatworms.Bioessays. 2004; 26: 1046-1057Crossref PubMed Scopus (109) Google Scholar, Hejnol and Martindale, 2008bHejnol A. Martindale M.Q. Acoel development supports a simple planula-like urbilaterian.Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2008; 363: 1493-1501Crossref PubMed Scopus (85) Google Scholar) and may not even represent the protostome-deuterostome ancestor (Lowe et al., 2003Lowe C.J. Wu M. Salic A. Evans L. Lander E. Stange-Thomann N. Gruber C.E. Gerhart J. Kirschner M. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system.Cell. 2003; 113: 853-865Abstract Full Text Full Text PDF PubMed Scopus (360) Google Scholar, Lowe et al., 2006Lowe C.J. Terasaki M. Wu M. Freeman Jr., R.M. Runft L. Kwan K. Haigo S. Aronowicz J. Lander E. Gruber C. et al.Dorsoventral patterning in hemichordates: insights into early chordate evolution.PLoS Biol. 2006; 4: e291Crossref PubMed Scopus (256) Google Scholar). Our deeper and more accurate understanding of the evolutionary relationships among animals no longer justifies the assumption that the deuterostome ancestor resembled a vertebrate chordate or that the protostome ancestor resembled a dipteran arthropod (Arendt and Nübler-Jung, 1997Arendt D. Nübler-Jung K. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates.Mech. Dev. 1997; 61: 7-21Crossref PubMed Scopus (130) Google Scholar, Carroll et al., 2001Carroll S.B. Grenier J.K. Weatherbee S.D. From DNA to Diversity. Blackwell Science, Malden2001Google Scholar, De Robertis, 2008De Robertis E.M. Evo-devo: variations on ancestral themes.Cell. 2008; 132: 185-195Abstract Full Text Full Text PDF PubMed Scopus (220) Google Scholar, De Robertis and Sasai, 1996De Robertis E.M. Sasai Y. A common plan for dorsoventral patterning in Bilateria.Nature. 1996; 380: 37-40Crossref PubMed Scopus (568) Google Scholar). Indeed, while many scientists assume that the relationships among living animals, the order, time, and position in which they arose, and hence the origin of distinct morphological features during evolution, have already been solved, this is not the case. Molecular approaches have, and continue to, radically change our understanding of animal evolution with profound implications regarding the direction of evolutionary change (see, e.g., Arendt and Nübler-Jung, 1994Arendt D. Nübler-Jung K. Inversion of dorsoventral axis?.Nature. 1994; 371: 26Crossref PubMed Scopus (226) Google Scholar, Arendt et al., 2001Arendt D. Technau U. Wittbrodt J. Evolution of the bilaterian larval foregut.Nature. 2001; 409: 81-85Crossref PubMed Scopus (186) Google Scholar, Denes et al., 2007Denes A.S. Jekely G. Steinmetz P.R. Raible F. Snyman H. Prud'homme B. Ferrier D.E. Balavoine G. Arendt D. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria.Cell. 2007; 129: 277-288Abstract Full Text Full Text PDF PubMed Scopus (309) Google Scholar, Finnerty et al., 2004Finnerty J.R. Pang K. Burton P. Paulson D. Martindale M.Q. Origins of bilateral symmetry: Hox and dpp expression in a sea anemone.Science. 2004; 304: 1335-1337Crossref PubMed Scopus (282) Google Scholar, Hejnol and Martindale, 2008aHejnol A. Martindale M.Q. Acoel development indicates the independent evolution of the bilaterian mouth and anus.Nature. 2008; 456: 382-386Crossref PubMed Scopus (97) Google Scholar, Lowe et al., 2006Lowe C.J. Terasaki M. Wu M. Freeman Jr., R.M. Runft L. Kwan K. Haigo S. Aronowicz J. Lander E. Gruber C. et al.Dorsoventral patterning in hemichordates: insights into early chordate evolution.PLoS Biol. 2006; 4: e291Crossref PubMed Scopus (256) Google Scholar). It has only been a decade (Aguinaldo et al., 1997Aguinaldo A.M. Turbeville J.M. Linford L.S. Rivera M.C. Garey J.R. Raff R.A. Lake J.A. Evidence for a clade of nematodes, arthropods and other moulting animals.Nature. 1997; 387: 489-493Crossref PubMed Scopus (1218) Google Scholar) since we realized that flies (arthropods) and nematodes are related to one another in a group called the Ecdysozoa (Figure 1), but these animals do not look similar. Did the common ancestor of these two groups have reiterated body segments, a mesodermally lined body cavity (called a coelom), and lateral appendages that were lost in the lineage that gave rise to the nematodes? Or, did these morphological features evolve independently in the arthropod line? In order to determine the features of the ecdysozoan ancestor, one also needs to know what the common ancestor of the lophotrochozoan group (Figure 1), which gave rise to animals as diverse as planarians, snails, and squids, looked like. And to understand the protostome ancestor, we need to know what the deuterostome ancestor that gave rise to sea urchins, sea squirts, and vertebrates was like. All these questions need to be answered first, before one can reconstruct the last common ancestor of the Bilateria, the iconic Urbilaterian. Recent phylogenetic studies incorporating a larger diversity of animal groups suggest that acoelomorph flatworms (Figure 1) are likely to share characteristics in common with the Urbilaterian (Ruiz-Trillo et al., 2004Ruiz-Trillo I. Riutort M. Fourcade H.M. Baguñá J. Boore J.L. Mitochondrial genome data support the basal position of Acoelomorpha and the polyphyly of the Platyhelminthes.Mol. Phylogenet. Evol. 2004; 33: 321-332Crossref PubMed Scopus (72) Google Scholar, Ruiz-Trillo et al., 1999Ruiz-Trillo I. Riutort M. Littlewood D.T.J. Herniou E.A. Baguñá J. Acoel flatworms: earliest extant bilaterian metazoans, not members of platyhelminthes.Science. 1999; 283: 1919-1923Crossref PubMed Scopus (337) Google Scholar, Telford et al., 2003Telford M.J. Lockyer A.E. Cartwright-Finch C. Littlewood D.T.J. Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms.Proc. R. Soc. Lond. B. Biol. Sci. 2003; 270: 1077-1083Crossref Scopus (116) Google Scholar, Wallberg et al., 2007Wallberg A. Curini-Galletti M. Ahmadzadeh A. Jondelius U. Dismissal of acoelomorpha: acoela and nemertodermatida are separate early bilaterian clades.Zool. Scr. 2007; 36: 509-523Crossref Scopus (59) Google Scholar). Acoelomorphs are small, direct developing (no larval form), unsegmented, ciliated, appendage-less worms. They have definitive mesoderm that forms muscle (but no coelom, circulatory, or excretory system), multiple parallel longitudinal nerve cords (i.e., no dorsally or ventrally “centralized” nervous system), and a single opening to the gut cavity (Bourlat and Hejnol, 2009Bourlat S.J. Hejnol A. Acoels.Curr. Biol. 2009; 19: R279-R280Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar, Haszprunar, 1996Haszprunar G. Plathelminthes and Plathelminthomorpha - paraphyletic taxa.J. Zool. Syst. Evol. Res. 1996; 34: 41-48Crossref Scopus (83) Google Scholar, Rieger et al., 1991Rieger R. Tyler S. Smith J.P.S. Rieger G.E. Platyhelminthes: Turbellaria.in: Harrison F.W. Bogitsch B.J. Microscopic Anatomy of Invertebrates. John Wiley & Sons, New York1991: 7-140Google Scholar). Animal groups that arose even earlier in metazoan evolution than bilaterians (Figure 1), such as the cnidarians (sea anemones, corals, and jellyfish), ctenophores (comb jellies), and sponges, also lack a through gut (with separate mouth and anus), a coelom, appendages, excretory system, reiterated body segments, and a (dorsally or ventrally) centralized nervous system, suggesting that the common ancestor of all bilaterian groups may have also lacked these features and raising the possibility that these morphological characteristics arose at least once, or perhaps multiple times, during metazoan diversification. These results illustrate a renewed importance of mapping morphological characters on to robust phylogenetic trees to determine the direction of evolutionary change. Total genome sequencing from a growing list of metazoans (e.g., Putnam et al., 2007Putnam N.H. Srivastava M. Hellsten U. Dirks B. Chapman J. Salamov A. Terry A. Shapiro H. Lindquist E. Kapitonov V.V. et al.Sea anemone genome reveals the gene repertoire and genomic organization of the eumetazoan ancestor.Science. 2007; 317: 86-94Crossref PubMed Scopus (1080) Google Scholar, Putnam et al., 2008Putnam N.H. Butts T. Ferrier D.E. Furlong R.F. Hellsten U. Kawashima T. Robinson-Rechavi M. Shoguchi E. Terry A. Yu J.K. et al.The amphioxus genome and the evolution of the chordate karyotype.Nature. 2008; 453: 1064-1071Crossref PubMed Scopus (1142) Google Scholar, Srivastava et al., 2008Srivastava M. Begovic E. Chapman J. Putnam N.H. Hellsten U. Kawashima T. Kuo A. Mitros T. Salamov A. Carpenter M.L. et al.The Trichoplax genome and the nature of placozoans.Nature. 2008; 454: 955-960Crossref PubMed Scopus (594) Google Scholar) has shown that there is no simple relationship between genomic/molecular complexity and organismal/developmental complexity, so the mere presence of members of conserved gene families (e.g., “segmentation genes”) reveals little about how they were deployed at different nodes of animal evolution. Understanding the true history of phylogenetic relationships of metazoan animals is thus of utmost importance for understanding the history of life on planet Earth because it could reveal whether certain features (e.g., coeloms, body segments, nerve cords, digestive system, etc.) previously thought to have characterized the Urbilaterian evolved independently in different animal lineages. Thus, a detailed understanding of the developmental basis for the formation of these structures in all different metazoan lineages is essential for understanding how molecular pathways were modified to generate the vast array of biological diversity in existence. While the complexity and modifications of organs and organ systems dominate discussion of bilaterian evolution, less attention has been focused on the initial evolutionary origin of these traits. Arguably the most profound change in body plan organization in the Metazoa occurred in the early animal lineages that gave rise to the Bilateria, where important traits like mesoderm, a condensed nervous system, and a clear bilateral body axis appeared from a morphologically much simpler animal (Schmidt-Rhaesa, 2007Schmidt-Rhaesa A. The Evolution of Organ Systems. Oxford University Press, Oxford2007Crossref Scopus (155) Google Scholar). Several scenarios formulated by different authors of the last century attempt to explain such a transition and try to combine the evolution of the body axes with the evolution of complex organ systems in the context of life history evolution. Virtually all scenarios that explain the evolution of the bilaterian body plan are versions of Haeckel's “Gastraea” theory (Haeckel, 1874Haeckel E. Die Gastraea-Theorie, die phylogenetische Classification des Thierreiches und die Homologie der Keimblätter.Jena. Z. Naturwiss. 1874; 8: 1-55Google Scholar), which posits a simple diploblastic organism composed of an ectodermally derived epidermis surrounding an endodermally derived blind gut with a single posterior opening to the outside world (e.g., mouth/anus) as the hypothetical precursor to all bilaterian forms. The anterior-posterior axis of this ancestral animal is defined by the direction of locomotion (e.g., the major swimming or crawling axis), with the differentiated neural/sensory structures at the leading pole being homologous with the anterior brain of extant bilaterians (Figure 2). A critical issue related to the developmental explanation for how more complex bilaterians arose from a bilayered organism is the site of gastrulation (the spatial position of presumptive endodermal gut tissue) and its relationship to the original opening to the gastric cavity of an ancestral metazoan relative to the direction of locomotion (Figure 2). In one scenario, the site of gastrulation (blastopore) of the ancestor remains as the posterior opening to the digestive tract (anus), with a new mouth evolving independently from an opening anteriorly (Figure 2A; see Lankester, 1877Lankester E.R. Notes on the embryology and classification of the animal kingdom: Comprising a revision of speculations relative to the origin and significance of germ layers.Q. J. Microsc. Soc. 1877; 17: 399-454Google Scholar). This developmental pattern is called deuterostomy and is seen in extant members of a large clade of animals including echinoderms, hemichordates, cephalochordates, and vertebrates (Deuterostomia) (Figure 1). Another idea, the Acoeloid-Planuloid hypothesis (Von Graff, 1891Von Graff L. Die Organisation der Turbellaria Acoela. von Wilhelm Engelmann, Leipzig1891Google Scholar), suggests that the blastoporal opening to blind gut originally occurred in the posterior region but then moved anteriorly along the ventral surface over evolutionary time (Figure 2C). This idea argues that the mouth is homologous in all animals and that the formation of a second opening to the gut, the anus, occurred secondarily (Figure 2) (Beklemishev, 1969Beklemishev W.N. Principles of Comparative Anatomy of Invertebrates. University of Chicago Press, Edinburgh1969Google Scholar, Hyman, 1951Hyman L.H. Platyhelminthes and Rhynchocoela, Volume II, The Invertebrates. McGraw-Hill, New York1951Google Scholar, Salvini-Plawen, 1978Salvini-Plawen L. On the origin and evolution of the lower Metazoa.J. Zoolog. Syst. Evol. Res. 1978; 16: 40-88Crossref Scopus (136) Google Scholar). A third hypothesis argues that a posterior opening to the gut of a “Gastraea”-like ancestral creature gives rise to both mouth and anus simultaneously by a process called amphistomy, in which a slit-like elongation of the blastopore followed by a lateral closure gives rise to openings at both ends of the through gut (Figure 2B) (Arendt and Nübler-Jung, 1997Arendt D. Nübler-Jung K. Dorsal or ventral: similarities in fate maps and gastrulation patterns in annelids, arthropods and chordates.Mech. Dev. 1997; 61: 7-21Crossref PubMed Scopus (130) Google Scholar, Malakhov, 2004Malakhov V.V. Zh. Obshch. Biol. 2004; 65: 371-388PubMed Google Scholar, Remane, 1950Remane A. Die Entstehung der Metamerie der Wirbellosen.Zool. Anz. 1950; : 18-23Google Scholar, Sedgwick, 1884Sedgwick W. On the origin of metameric segmentation and some other morphological questions.Q. J. Microsc. Sci. 1884; 24: 43-82Google Scholar). Clearly, these theories cannot all be correct and each has a distinct set of predictions relative to the developmental basis for bilaterian body plan evolution. All these theories rely heavily on observations of cnidarian development, the well-accepted sister group to the Bilateria (Figure 1). Cnidarians possess a swimming ciliated planula stage (Figure 3) in which the site of gastrulation (and the future mouth opening) is located at the posterior (trailing) pole of the swimming direction and a neural structure (called the apical tuft), tacitly assumed to be homologous with the bilaterian brain (Nielsen, 1999Nielsen C. Origin of the chordate central nervous system - and the origin of chordates.Dev. Genes Evol. 1999; 209: 198-205Crossref PubMed Scopus (92) Google Scholar, Nielsen, 2005aNielsen C. Larval and adult brains.Evol. Dev. 2005; 7: 483-489Crossref PubMed Scopus (61) Google Scholar), is located at the leading end. We will demonstrate in this review that most of these concepts of metazoan evolution are not consistent with the developmental data recently obtained from diverse animals. While the previous hypotheses were based on larval morphology and the swimming/crawling direction as the major axial organizing system, we here argue that developmental phenomena organized around the animal-vegetal axis delivers more insights into the developmental modifications that lead to evolutionary transitions of body plan organization in the stem lineage of the Bilateria. All metazoan embryos arise from products of meiosis. Oogenesis and spermatogenesis are among the unifying apomorphies for the Metazoa (Ax, 1996Ax P. Multicellular Animals. A New Approach to the Phylogenetic Order in Nature. Volume I. Springer, Berlin1996Google Scholar). In the oocyte, the position where the meiotic reduction divisions generate polar bodies is defined as the animal pole of the primary (animal-vegetal) egg axis and, thus, can be used as a reference point for comparing the axial relationships of metazoan embryos. Although detailed information is lacking in many animal groups, in cnidarians (Eckelbarger et al., 2008Eckelbarger K.J. Hand C. Uhlinger K.R. Ultrastructural features of the trophonema and oogenesis in the starlet sea anemone, Nematostella vectensis (Edwardsiidae).Invertebr. Biol. 2008; 127: 381-395Crossref Scopus (21) Google Scholar), dipteran flies (Gilbert and Raunio, 1997Gilbert S.F. Raunio A.M. Embryology. Constructing the Organism. Sinauer Associates, Inc., Sunderland, MA1997Google Scholar), and echinoids (Frick and Ruppert, 1996Frick J.E. Ruppert E.E. Primordial germ cells of Synaptula hydriformis (Holothuroidea; Echinodermata) are epithelial flagellated-collar cells: Their apical-basal polarity becomes primary egg polarity.Biol. Bull. 1996; 191: 168-177Crossref Scopus (16) Google Scholar, Frick et al., 1996Frick J.E. Ruppert E.E. Wourms J.P. Morphology of the ovotestis of Synaptula hydriformis (Holothuroidea, Apoda): An evolutionary model of oogenesis and the origin of egg polarity in echinoderms.Invertebr. Biol. 1996; 115: 46-66Crossref Scopus (24) Google Scholar) the animal pole normally corresponds to the position where the oocyte makes contact with its germinative epithelium, suggesting that the conditions for establishing axial embryonic polarity in these embryos are set up maternally. In virtually all investigated bilaterian embryos, fate mapping experiments have shown that subsequent development is organized along this primary egg axis (Goldstein and Freeman, 1997Goldstein B. Freeman G. Axis specification in animal development.Bioessays. 1997; 19: 105-116Crossref PubMed Scopus (63) Google Scholar, Wall, 1990Wall R. This Side Up. Spatial Determination in the Early Development of Animals. Cambridge University Press, Cambridge1990Crossref Google Scholar). For example, the site of gastrulation (the place where endoderm and/or endomesoderm is generated), the location of the mouth, head region, appendages, etc., are generated from predictable places corresponding to their position along the animal-vegetal axis. There are examples throughout the metazoan tree, including ctenophores, acoelomorphs, chordates, spiralians, and ecdysozoans, in which the stereotypy of embryonic development along the animal-vegetal axis allows the prediction of the exact fate of identified blastomeres (Gilbert and Raunio, 1997Gilbert S.F. Raunio A.M. Embryology. Constructing the Organism. Sinauer Associates, Inc., Sunderland, MA1997Google Scholar). Thus, consideration of the primary egg axis is likely to provide important landmarks for changes related to the evolution of developmental patterning. When considering the role of the primary egg axis in the elaboration of body plans during early animal evolution, two taxa, ctenophores and cnidarians, are particularly relevant (Figure 1). Although poriferans (sponges) and placozoans (Trichoplax) branch near the base of the Metazoa (Figure 1), their body plans are difficult to compare with other metazoans, and their embryos, when present, are technically difficult to study. For example, adult sponges and placazoans do not display an obvious anterior-posterior axis either morphologically or behaviorally, and the developmental origin of germ layers (i.e., gastrulation) relative to the embryonic (i.e., animal-vegetal) axis or the adult body plan is not clear. Without these important details, these taxa are not likely to provide much additional insight into the evolution of bilaterian body plans. Ctenophores (e.g., comb jellies) and cnidarians, in particular, anthozoan cnidarians (e.g., sea anemones, corals, sea fans, and sea whips) with their simple life history, are important because they have a major longitudinal body axis and definitive guts that can be homologized to bilaterians. Furthermore, their early development can be studied in detail with relationship to their adult axial properties (Fritzenwanker et al., 2007Fritzenwanker J.H. Genikhovich G. Kraus Y. Technau U. Early development and axis specification in the sea anemone Nematostella vectensis.Dev. Biol. 2007; 310: 264-279Crossref PubMed Scopus (84) Google Scholar, Lee et al., 2007Lee P.N. Kumburegama S. Marlow H.Q. Martindale M.Q. Wikramanayake A.H. Asymmetric developmental potential along the animal-vegetal axis in the anthozoan cnidarian, Nematostella vectensis, is mediated by Dishevelled.Dev. Biol. 2007; 310: 169-186Crossref PubMed Scopus (90) Google Scholar, Martindale and Henry, 1999Martindale M.Q. Henry J.Q. Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages.Dev. Biol. 1999; 214: 243-257Crossref PubMed Scopus (85) Google Scholar). All recent molecular phylogenomic studies agree that cnidarians are the sister group to all other bilaterians (Figure 1), and some suggest that ctenophores (not sponges) form the earliest branch in the metazoan lineage (Dunn et al., 2008Dunn C.W. Hejnol A. Matus D.Q. Pang K. Browne W.E. Smith S.A. Seaver E. Rouse G.W. Obst M. Edgecombe G.D. et al.Broad phylogenomic sampling improves resolution of the animal tree of life.Nature. 2008; 452: 745-749Crossref PubMed Scopus (1397) Google Scholar). Even if the phylogenetic relationship of ctenophores relative to other metazoans is revised, the similarities in egg organization and axial properties of ctenophores and cnidarians as groups branching prior to the radiation of bilaterians suggest that something can be learned about the developmental basis for the origin of ancestral character states from these groups of animals. These two uniquely distinct taxa could, therefore, bracket (Figure 1) important early events in metazoan evolution and provide insight into the developmental basis for body plan evolution. Vital dye labeling of defined regions/blastomeres in developing embryos allows one to predict the eventual fates of these regions in the resultant larval or juvenile adult body plan. Fate mapping experiments in cnidarians and ctenophore embryos have allowed three important facts to be defined. First, the animal pole (defined by the site of polar body formation) in both ctenophore (Freeman, 1977Freeman G. The establishment of the oral-aboral axis in the ctenophore embryo.J. Embryol. Exp. Morphol. 1977; 42: 237-260Google Scholar, Martindale and Henry, 1999Martindale M.Q. Henry J.Q. Intracellular fate mapping in a basal metazoan, the ctenophore Mnemiopsis leidyi, reveals the origins of mesoderm and the existence of indeterminate cell lineages.Dev. Biol. 1999; 214: 243-257Crossref PubMed Scopus (85) Google Scholar) and cnidarian embryos (Freeman, 1981bFreeman G. The role of polarity in the development of the hydrozoan planula larva.Rouxs Arch. Dev. Biol. 1981; 190: 168-184Crossref Scopus (59) Google Scholar, Momose and Schmid, 2006Momose T. Schmid V. Animal pole determinants define oral-aboral axis polarity and endodermal cell-fate in hydrozoan jellyfish Podocoryne carnea.Dev. Biol. 2006; 292: 371-380Crossref PubMed Scopus (33) Google Scholar, Schlawny and Pfannenstiel, 1991Schlawny A. Pfannenstiel H.D. Prospective fate of early blastomeres in Hydractinia echinata (Cnidaria, Hydrozoa).Dev. Genes Evol. 1991; 200: 143-148Google Scholar, Tessier, 1931Tessier G. Étude expérimentale du développement de quelques hydraires.Ann. Sci. Nat. Ser. X. 1931; 14: 5-60Google Scholar) is normally the site of the formation of the unipolar first cleavage furrow, which corresponds to the oral pole that gives rise to the future mouth of both adult ctenophores and cnidarian polyps (Figure 3). Furthermore, in both clades it has been shown experimentally that the site of first cleavage is causally involved with the formation of the oral-aboral axis (Freeman, 1977Freeman G. The establishment of the oral-aboral axis in the ctenophore embryo.J. Embryol. Exp. Morphol. 1977; 42: 237-260Google Scholar, Freeman, 1981bFreeman G. The role of polarity in the development of the hydrozoan planula larva.Rouxs Arch. Dev. Biol. 1981; 190: 168-184Crossref Scopus (59) Google Scholar). If the zygotic nucleus is moved from the original animal pole to an ectopic site by gentle centrifugation, a new oral-aboral axis is established, with the new site of first cleavage determining the future oral pole (Figure 3). Drug treatments that generate two simultaneous cleavage furrows in cnidarian embryos generate two mouths, indicating that the site of first cleavage plays an important role in organizing the future oral opening (Freeman, 1981aFreeman G. The cleavage initiation site establishes the posterior pole of the hydrozoan embryo.Rouxs Arch. Dev. Biol. 1981; 190: 123-125Crossref Scopus (33) Google Scholar). These experiments show that although there might be a consistent relationship of the primary egg axis to future developmental events that are set up maternally, they merely establish the conditions for the formation of the first cleavage furrow. Thus, unlike most other bilaterians, both the definitive embryonic and