New ideas on the origin of bilateral animals

Comparative anatomy and embryology provide impressive evidence that the ventral side of all Bilateria (except Chordata) originates from the blastoporal surface, while the mouth and anus develop, respectively, from the anterior and posterior extremities of an elongated blastopore. From the point of view of paleontology, some Vendian multicellular animals represent transitional forms between Radiata and Bilateria. Vendian Bilateria are metameric organisms with a symmetrical or asymmetrical arrangement of segments; they can be considered as bilaterally symmetrical coelenterates crawling on the oral surface. In the recent Cnidaria, homologues of the genes “Brachyury,” “goosecoid” and “fork head” are expressed around the mouth. In the recent Bilateria these genes are expressed along the elongated blastopore and around the mouth and anus. These data corroborate the validity of the idea of amphistomy and the homology between the ventral surface in Bilateria and oral disk in coelenterates. It is supposed that the ancestors of Bilateria were crawling on the oral surface (=ventral side) and gave rise to both Fanerozoic Cnidaria and triploblastic Bilateria. This allows us to suggest the origin of Bilateria from Vendian bilaterally symmetrical coelenterates with numerous metameric pockets of the gastral cavity. Such ancestors gave rise to both Cnidaria and Bilateria. Apparently the primary Bilateria were complicated organisms having a coelom and segmentation, which allows us to explain the great diversity of highly organized organisms (arthropods, mollusks, and others) in the Cambrian era. An idea is proposed that Ctenophora are the only group of recent Eumetazoa that retain primary axial symmetry.     

Evolution of deuterostomy – and origin of the chordates

The chordates are usually characterized as bilaterians showing deuterostomy, i.e. the mouth developing as a new opening between the archenteron and the ectoderm, serial gill pores/slits, and the complex of chorda and neural tube. Both numerous molecular studies and studies of morphology and embryology demonstrate that the neural tube must be considered homologous to the ventral nerve cord(s) of the protostomes, but the origin of the ‘new’ mouth of the deuterostomes has remained enigmatic. However, deuterostomy is known to occur in several protostomian groups, such as the chaetognaths and representatives of annelids, molluscs, arthropods and priapulans. This raises the question whether the deuterostomian mouth is in fact homologous with that of the protostomes, viz. the anterior opening of the ancestral blastopore divided through lateral blastopore fusion, i.e. amphistomy. A few studies of gene expression show identical expression patterns around mouth and anus in protostomes and deuterostomes. Closer studies of the embryology of ascidians and vertebrates show that the mouth/stomodaeum differentiates from the anterior edge of the neural plate. Together this indicates that the chordate mouth has moved to the anterior edge of the blastopore, so that the anterior loop of the ancestral circumblastoporal nerve cord, which is narrow in the protostomes, has become indistinguishable. In the vertebrates, the mouth has moved further around the anterior pole to the ‘ventral’ side. The conclusion must be that the chordate mouth (and that of the deuterostomes in general) is homologous to the protostomian mouth and that the latest common ancestor of protostomes and deuterostomes developed through amphistomy, as suggested by the trochaea theory.     

Larval and adult brains

Apical organs are a well-known structure in almost all ciliated eumetazoan larvae, although their function is poorly known. A review of the literature indicates that this small ganglion is the "brain" of the early larva, and it seems probable that it represents the brain of the ancestral, holopelagic ancestor of all eumetazoans, the gastraea. This early brain is lost before or at metamorphosis in all groups. Protostomes (excluding phoronids and brachiopods) appear to have brains of dual origin. Their larvae develop a pair of cephalic ganglia at the episphere lateral to the apical organ, and these two ganglia become an important part of the adult brain. The episphere and the cerebral ganglia show Otx expression, whereas Hox gene expression has not been seen in this part of the brain. A ventral nervous system develops around the blastopore, which becomes divided into mouth and anus by fusion of the lateral blastopore lips. The circumblastoporal nerve ring becomes differentiated into a nerve ring around the mouth, becoming part of the adult brain, a pair of ventral nerve cords, in some cases differentiated into a chain of ganglia, and a ring around the anus. This part of the nervous system appears to be homologous with the oral nerve ring of cnidarians. This interpretation is supported by the expression of Hox genes around the cnidarian mouth and in the ventral nervous system of the protostomes. The development of phoronids, brachiopods, echinoderms, and enteropneusts does not lead to the formation of an episphere or to differentiation of cerebral ganglia. In general, a well-defined brain is lacking, and Hox genes are generally not expressed in the larval organs, although this has not been well studied.     

Symmetry and the tentacular apparatus in Cnidaria

Comparative analysis provides evidence that bilateral symmetry is a primary character of Cnidaria. All anthozoan taxa are characterized by bilateral symmetry. The anthozoan pharyngeal plane is a plane of bilateral symmetry of mesenteries and, at the same time, it is a plane of bilateral symmetry of regulatory gene expression in anthozoan morphogenesis. In Medusozoa, the bilateral symmetry is replaced by radial symmetry, but some hydrozoans (for example, Corymorphidae) demonstrate bilateral symmetry. The bilateral symmetry of Cnidaria is thought to be inherited from the common ancestors of both cnidarians and triploblastic bilaterians. The secondary radial symmetry of Cnidaria evidently is a result of the adaptation to the sessile mode of life. The presence of both the marginal and labial rings of tentacles is supposed to be a plesiomorphic character of Cnidaria. In some groups of cnidarians, one of the tentacle rings may be reduced.     

The origins of axial patterning in the metazoa: how old is bilateral symmetry?

Bilateral symmetry is a hallmark of the Bilateria. It is achieved by the intersection of two orthogonal axes of polarity: the anterior-posterior (A-P) axis and the dorsal-ventral (D-V) axis. It is widely thought that bilateral symmetry evolved in the common ancestor of the Bilateria. However, it has long been known that members of the phylum Cnidaria, an outgroup to the Bilateria, also exhibit bilateral symmetry. Recent studies have examined the developmental expression of axial patterning genes in members of the phylum Cnidaria. Hox genes play a conserved role in patterning the A-P axis of bilaterians. Hox genes are expressed in staggered axial domains along the oral-aboral axis of cnidarians, suggesting that Hox patterning of the primary body axis was already present in the cnidarian-bilaterian ancestor. Dpp plays a conserved role patterning the D-V axis of bilaterians. Asymmetric expression of dpp about the directive axis of cnidarians implies that this patterning system is similarly ancient. Taken together, these result imply that bilateral symmetry had already evolved before the Cnidaria diverged from the Bilateria.     

Components of both major axial patterning systems of the Bilateria are differentially expressed along the primary axis of a 'radiate' animal, the anthozoan cnidarian Acropora millepora

Cnidarians are animals with a single (oral/aboral) overt body axis and with origins that nominally predate bilaterality. To better understand the evolution of axial patterning mechanisms, we characterized genes from the coral, Acropora millepora (Class Anthozoa) that are considered to be unambiguous markers of the bilaterian anterior/posterior and dorsal/ventral axes. Homologs of Otx/otd and Emx/ems, definitive anterior markers across the Bilateria, are expressed at opposite ends of the Acropora larva; otxA-Am initially around the blastopore and later preferentially toward the oral end in the ectoderm, and emx-Am predominantly in putative neurons in the aboral half of the planula larva, in a domain overlapping that of cnox-2Am, a Gsh/ind gene. The Acropora homologs of Pax-3/7, NKX2.1/vnd and Msx/msh are expressed in axially restricted and largely non-overlapping patterns in larval ectoderm. In Acropora, components of both the D/V and A/P patterning systems of bilateral animals are therefore expressed in regionally restricted patterns along the single overt body axis of the planula larva, and two 'anterior' markers are expressed at opposite ends of the axis. Thus, although some specific gene functions appear to be conserved between cnidarians and higher animals, no simple relationship exists between axial patterning systems in the two groups.     

Deuterostomic Development in the Protostome Priapulus caudatus

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Highlights? In the protostome P. caudatus, the blastopore forms the anus (deuterostomy) ? The hindgut markers brachyury and cdx are expressed in the blastopore and in the anus ? The foregut markers foxA and gsc are detected in the mouth, but not in the blastopore ? Results favor deuterostomy in ecdysozoan, protostome, and bilaterian ancestors     

Back in time: a new systematic proposal for the Bilateria

Conventional wisdom suggests that bilateral organisms arose from ancestors that were radially, rather than bilaterally, symmetrical and, therefore, had a single body axis and no mesoderm. The two main hypotheses on how this transformation took place consider either a simple organism akin to the planula larva of extant cnidarians or the acoel Platyhelminthes (planuloid-acoeloid theory), or a rather complex organism bearing several or most features of advanced coelomate bilaterians (archicoelomate theory). We report phylogenetic analyses of bilaterian metazoans using quantitative (ribosomal, nuclear and expressed sequence tag sequences) and qualitative (HOX cluster genes and microRNA sets) markers. The phylogenetic trees obtained corroborate the position of acoel and nemertodermatid flatworms as the earliest branching extant members of the Bilateria. Moreover, some acoelomate and pseudocoelomate clades appear as early branching lophotrochozoans and deuterostomes. These results strengthen the view that stem bilaterians were small, acoelomate/pseudocoelomate, benthic organisms derived from planuloid-like organisms. Because morphological and recent gene expression data suggest that cnidarians are actually bilateral, the origin of the last common bilaterian ancestor has to be put back in time earlier than the cnidarian-bilaterian split in the form of a planuloid animal. A new systematic scheme for the Bilateria that includes the Cnidaria is suggested and its main implications discussed.     

Transformations of the axial complex of ophiuroids as a result of shifting of the madreporite to the oral side

In comparison with Asteroidea, the axial complex of ophiuroids has some important features, which are the result of shifting of the madreporite from the aboral side to the oral side. In contrast to Asteroidea, the stone canal of ophiuroids connects with the water ring from the outside, not from the inside. In Ophiuroidea, the somatocoelomic perihaemal coelom is closer to the mouth than the axocoelomic ring. The water ring of ophiuroids is shifted to the oral side relative to the perihaemal coelomic rings. The genital coelom and gastric haemal ring are located on the outer side of the axial complex, whereas in Asteroidea, they are located on the inner side. The pericardial part of the axial organ is situated on the oral side. The interradial sections of the genital coelom and genital haemal ring are descended to the oral side. Our hypothesis considers that the ancestors of ophiuroids turned the aboral side of the animal to the substratum. It caused shifting of the madreporite to the oral side and closing of the anus.     

The aboral pore of hydra: evidence that the digestive tract of hydra is a tube not a sac

The digestive tract of Bilateria is a tube with a mouth at one end and an anus at the other end. Radiata, that include the phylum Cnidaria, have a blind-sac form of digestive tract with only one opening. It has therefore been commonly believed that the evolution of the body plan from Radiata to Bilateria included the change of the digestive tract from a blind sac to a tube. In this study, we report that there is a very narrow opening at the aboral end of hydra termed the aboral pore. This confirms a classical finding by Kanajew (Zool Anz, 76:37-44, 1928), but we confirmed it in both asexually reproduced and sexually reproduced polyps, demonstrating that the aboral pore represents innate morphology. We also find that the opening coincides with the site where synthesis of an extracellular matrix-degrading enzyme, hydra matrix metalloprotease, is elevated suggesting that the pore is maintained by extracellular matrix degradation. Finally, we find that there is material transfer through the opening in both inward and outward directions. From these observations, we conclude that the digestive tract and the body plan of hydra is not a blind sac as formerly believed but is a tube with a tapered end.     

Animal phylogeny in the light of the trochaea theory

Ultrastructural similarities unite Choanoflagellata and Metazoa as the Kingdom Animalia. Mctazoa (Porifera + Placozoa + Gastraeozoa) are characterized by the presence of collagen, septate/tight junctions and spermatozoa. Porifera and Placozoa lack basal lamina, nerve cells and synapses, which characterize Gastraeozoa (Cnidaria + Trochaeozoa). Gnidaria have cnidoblasts and lack the multiciliate cells found in almost all Trochaeozoa (Gastroneuralia + Protornaeozoa). Gastroneuralia (Spiralia + Aschelminthes) have an apical brain and a pair of ventral nerves, a blastopore which becomes mouth and anus, a mouth surrounded by a downstream collecting system of compound cilia, and a mesoderm formed from the blastopore lips. Spiralia (Articulata + Parenchymia + Bryozoa) have spiral cleavage and 4d-cell mesoderm, whereas these characters are lacking in Aschelminthes, which all lack primary larvae. Protornaeozoa (Ctenophora + Notoneuralia) have mesoderm from vegetal cells. Ctenophores have colloblasts. Notoneuralia have a dorsal nervous system behind the apical area and form a new mouth surrounded by an upstream collecting system of single cilia on monociliate cells; the blastopore becomes the anus surrounded by a ring of compound cilia.
These features fit the trochaea theory, which proposes that Gastroneuralia and Notoneuralia evolved independently from the trochaea, a blastaea with the blastopore surrounded by a ring of compound cilia, which were both locomotory and particle collecting.     

Evidence for a microRNA expansion in the bilaterian ancestor

Understanding how animal complexity has arisen and identifying the key genetic components of this process is a central goal of evolutionary developmental biology. The discovery of microRNAs (miRNAs) as key regulators of development has identified a new set of candidates for this role. microRNAs are small noncoding RNAs that regulate tissue-specific or temporal gene expression through base pairing with target mRNAs. The full extent of the evolutionary distribution of miRNAs is being revealed as more genomes are scrutinized. To explore the evolutionary origins of metazoan miRNAs, we searched the genomes of diverse animals occupying key phylogenetic positions for homologs of experimentally verified human, fly, and worm miRNAs. We identify 30 miRNAs conserved across bilaterians, almost double the previous estimate. We hypothesize that this larger than previously realized core set of miRNAs was already present in the ancestor of all Bilateria and likely had key roles in allowing the evolution of diverse specialist cell types, tissues, and complex morphology. In agreement with this hypothesis, we found only three, conserved miRNA families in the genome of the sea anemone Nematostella vectensis and no convincing family members in the genome of the demosponge Reniera sp. The dramatic expansion of the miRNA repertoire in bilaterians relative to sponges and cnidarians suggests that increased miRNA-mediated gene regulation accompanied the emergence of triploblastic organ-containing body plans. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Colonial origin for Emetazoa: major morphological transitions and the origin of bilaterian complexity

A new hypothesis for the evolution of Bilateria is presented. It is based on a reinterpretation of the morphological characters shared by protostomes and deuterostomes, which, when taken together with developmental processes shared by the two lineages, lead to the inescapable conclusion that the last common ancestor of Bilateria was complex. It possessed a head, a segmented trunk, and a tail. The segmented trunk was further divided into two sections. A dorsal brain innervated one or more sensory cells, which included photoreceptors. "Appendages" or outgrowths were present. The bilaterian ancestor also possessed serially repeated "segments" that were expressed ontogenetically as blocks of mesoderm or somites with adjoining fields of ectoderm or neuroectoderm. It displayed serially repeated gonads (gonocoels), each with a gonoduct and gonopore to the exterior, and serially repeated "coeloms" with connections to both the gut and the exterior (gill slits and pores). Podocytes, some of which were serially repeated in the trunk, formed sites of ultrafiltration. In addition, the bilaterian ancestor had unsegmented coeloms and a contractile blood vessel or "heart" formed by coelomic myoepithelial cells. These cells and their underlying basement membrane confine the hemocoelic fluid, or blood, in the connective tissue compartment. A possible scenario to account for this particular suite of characters is one in which a colony of organisms with a cnidarian grade of organization became individuated into a new entity with a bilaterian grade of organization. The transformation postulated encompassed three major transitions in the evolution of animals. These transitions included the origins of Metazoa, Eumetazoa, and Bilateria and involved the successive development of poriferan, cnidarian, and bilaterian grades of organization. Two models are presented for the sponge-to-cnidarian transition. In both models the loss of a flow-through pattern of water circulation in poriferans and the establishment of a single opening and epithelia sensu stricto in cnidarians are considered crucial events. In the model offered for the cnidarian-to-bilaterian transition, the last common ancestor of Eumetazoa is considered to have had a colonial, cnidarian-grade of organization. The ancestral cnidarian body plan would have been similar to that exhibited by pennatulacean anthozoans. It is postulated that a colonial organization could have provided a preadaptive framework for the evolution of the complex and modularized body plan of the triploblastic ancestor of Bilateria. Thus, one can explore the possibility that problematica such as ctenophores, the Ediacaran biota, archaeocyaths, and Yunnanozoon reflect the fact that complexity originated early and involved the evolution of a macroscopic compartmented ancestor. Bilaterian complexity can be understood in terms of Beklemishev "cycles" of duplication and colony individuation. Two such cycles appear to have transpired in the early evolution of Metazoa. The first gave rise to a multicellular organism with a sponge grade of organization and the second to the modularized ancestor of Bilateria. The latter episode may have been favored by the ecological conditions in the late Proterozoic. Whatever its cause, the individuation of a cnidarian-grade colony furnishes a possible explanation for the rapid diversification of bilaterians in the late Vendian and Cambrian. The creation of a complex yet versatile prototype, which could be rapidly modified by selection into a profusion of body plans, is postulated to have affected the timing, mode, and extent of the "Cambrian explosion." During the radiations, selective loss or simplification may have been as creative a force as innovation. Finally, colony individuation may have been a unique historical event that imprinted the development of bilaterians as the zootype and phylotypic stage. (ABSTRACT TRUNCATED)     

Identification of chaetognaths as protostomes is supported by the analysis of their mitochondrial genome

Determining the phylogenetic position of enigmatic phyla such as Chaetognatha is a longstanding challenge for biologists. Chaetognaths (or arrow worms) are small, bilaterally symmetrical metazoans. In the past decades, their relationships within the metazoans have been strongly debated because of embryological and morphological features shared with the two main branches of Bilateria: the deuterostomes and protostomes. Despite recent attempts based on molecular data, the Chaetognatha affinities have not yet been convincingly defined. To answer this fundamental question, we determined the complete mitochondrial DNA genome of Spadella cephaloptera. We report three unique features: it is the smallest metazoan mitochondrial genome known and lacks both atp8 and atp6 and all tRNA genes. Furthermore phylogenetic reconstructions show that Chaetognatha belongs to protostomes. This implies that some embryological characters observed in chaetognaths, such as a gut with a mouth not arising from blastopore (deuterostomy) and a mesoderm derived from archenteron (enterocoely), could be ancestral features (plesiomorphies) of bilaterians.     

T-box and homeobox genes from the ctenophore Pleurobrachia pileus: comparison of Brachyury, Tbx2/3 and Tlx in basal metazoans and bilaterians

Most animals are classified as Bilateria and only four phyla are still extant as outgroups, namely Porifera, Placozoa, Cnidaria and Ctenophora. These non-bilaterians were not considered to have a mesoderm and hence mesoderm-specific genes. However, the T-box gene Brachyury could be isolated from sponges, placozoans and cnidarians. Here, we describe the first Brachyury and a Tbx2/3 homologue from a ctenophore. In addition, analysing T-box and homeobox genes under comparable conditions in all four basal phyla lead to the discovery of novel T-box genes in sponges and cnidarians and a Tlx homeobox gene in the ctenophore Pleurobrachia pileus. The conservation of the T-box and the homeobox genes suggest that distinct subfamilies with different roles in bilaterians were already split in non-bilaterians.     

Embryogenesis in the reef-building coral Acropora spp

Embryogenesis in the reef building corals Acropora intermedia, A. solitaryensis, A. hyacinthus, A. digitifera, and A. tenuis was studied in detail at the morphological level, and the relationships among the animal pole, blastopore, and mouth were investigated for the first time in corals. These species showed essentially the same sequence of development. The embryo undergoes spiral-like holoblastic cleavage despite the presence of a dense isolecithal yolk. After the morula stage, the embryo enters the "prawn-chip" stage, which consists of an irregularly shaped cellular bilayer. The embryo begins to roll inward to form the bowl stage; the round shape observed during this stage suggests that it may be the beginning of gastrulation. However, the blastopore closes and the stomodeum (mouth and pharynx) is formed via invagination at a site near the closed blastopore. During the planula stage, a concavity forms in the aboral region in conjunction with numerous spirocysts, suggesting that spirocysts are used to attach to the substrate before the onset of metamorphosis.     

The Development of Radial and Biradial Symmetry: The Evolution of Bilaterality

SYNOPSIS. Understanding the evolutionary origin of novel metazoanbody plans continues to be one of the most sought after answersin biology. Perhaps the most profound change that may have occurredin the Metazoa is the appearance of bilaterally symmetricalforms from a presumably radially symmetrical ancestor. The symmetryproperties of bilaterally symmetrical larval and adult metazoansare generally set up during the cleavage period while most "radially"symmetrical cnidarians do not display a stereotyped cleavageprogram. Ctenophores display biradial symmetry and may representone intermediate form in the transition to bilateral symmetry.The early development of cnidarians and ctenophores is comparedwith respect to the timing and mechanisms of axial determination.The origin of the dorsal-ventral axis, and indeed the relationshipsof the major longitudinal axes, in cnidarians, ctenophores,and bilaterian animals are far from certain. The realizationthat many of the molecular mechanisms of axial determinationare conserved throughout the Bilateria allows one to formulatea set of predictions as to their possible role in the originsof bilaterian ancestors.