Did internal transport,rather than directed locomotion,favor the evolution of bilateral symmetry in animals?

The standard explanation for the origin of bilateral symmetry is that it conferred an advantage over radial symmetry for directed locomotion. However, recent developmental and phylogenetic studies suggest that bilateral symmetry may have evolved in a sessile benthic animal, predating the origin of directed locomotion. An evolutionarily feasible alternative explanation is that bilateral symmetry evolved to improve the efficiency of internal circulation by affecting the compartmentalization of the gut and the location of major ciliary tracts. This functional design principle is illustrated best by the phylum Cnidaria where symmetry varies from radial to tetraradial, biradial and bilateral. In the Cnidaria, bilateral symmetry is manifest most strongly in the internal anatomy and the disposition of ciliary tracts. Furthermore, the bilaterally symmetrical Cnidaria are typically sessile and, in those bilaterally symmetrical cnidarians that undergo directed locomotion, the secondary body axis does not bear a consistent orientation to the direction of locomotion as it typically does in Bilateria. Within the Cnidaria, the hypothesized advantage of bilateral symmetry for internal circulation can be tested by experimental analysis and computer modeling of fluid mechanics. The developmental evolution of symmetry within the Cnidaria can be further explored through comparative gene expression studies among species whose symmetry varies.     

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.     

Dead-end evolution of the Cnidaria as deduced from 5S ribosomal RNA sequences

Using nucleotide sequences of 5S ribosomal RNAs from 2 hydrozoan jellyfishes, 3 scyphozoan jellyfishes and 2 sea anemones, a phylogenetic tree of Cnidaria has been constructed to elucidate the evolutionary relationships of radial and bilateral symmetries. The 3 classes of Cnidaria examined herein belong to one branch, which does not include other metazoan phyla such as the Platyhelminthes. The Hydrozoa (having radial symmetry without septa) and the Scyphozoa (having radial symmetry with septa) are more closely related to each other than to the Anthozoa (having bilateral symmetry with septa). In classical taxonomy, multicellular animals are considered to have evolved through organisms with radial symmetry (e.g., Cnidaria) to bilateral symmetry. Our results, however, indicate that the emergence of the Bilateria was earlier than that of the Radiata, suggesting (in opposition to Haeckel's view) that the radial symmetry of Cnidaria is an evolutionary dead end.     

Early evolution of symmetry and polarity in metazoan body plans

The early diverging metazoan lineages have highly disparate adult body plan geometries, which can be characterised in terms of five major types of symmetry (asymmetrical, spherical, cylindrical, n-radial, bilateral). Patterns of evolutionary changes in symmetry types and the homology of body axes across lineages are discussed here by confronting evidence from comparative anatomy, phylogeny, genomics and evo-devo. The conventional scenario, postulating a graded complexification from asymmetry to radial and finally bilateral symmetry, is considered untenable. Cylindrical symmetry is likely to be the ancestral type from which derived all remaining types through multiple convergences. Recent proposals prompted by molecular data that the bilateral anatomies of many cnidarians and of the Bilateria are homologous are clearly not supported. The Hox-based patterning system operating along the antero-posterior axis of the Bilateria does not seem to predate their divergence with the Cnidaria, but intercellular signalling systems, notably the Wnt pathway, could have been involved in generating the main body axis in the last common ancestor of the Metazoa. To cite this article: M. Manuel, C. R. Biologies 332 (2009).     

Diverse radial symmetry among the Cambrian Fortunian fossil embryos from northern Sichuan and southern Shaanxi provinces,South China

The Cambrian Fortunian fossil embryos exhibit embryonic development of ancient animals and hence have important bearings on evolutionary developmental biology. They have radial symmetry, and may be early representatives of cnidarians. Here we report new material of three-dimensionally phosphatized fossil embryos from the Fortunian Kuanchuanpu Formation and coeval strata in northern Sichuan and southern Shaanxi provinces, South China. The new material includes previously reported fossil embryos assignable to Pseudooides prima with biradial symmetry or pseudo-hexaradial symmetry, Quadrapyrgites quadratacris with tetraradial symmetry, and Olivooides multisulcatus with pentaradial symmetry. Additionally, we recovered two new types of fossil embryos, i.e., Embryo I with hexaradial symmetry and Embryo II with octaradial symmetry, and they are tentatively suggested to represent new cnidarians. In contrast to the diverse radial symmetry of the Fortunian cnidarians, modern cnidarians exhibit stable tetraradial symmetry in medusozoans, biradial symmetry in anthozoans, and bilateral symmetry in siphonophores (Hydrozoa). The current study supports the view that the tetraradial symmetry of modern medusozoans is a surviving remnant of their Fortunian relatives.     

Shared antigenicity between the polar filaments of myxosporeans and other Cnidaria

Nematocysts containing coiled polar filaments are a distinguishing feature of members of the phylum Cnidaria. As a first step to characterizing the molecular structure of polar filaments, a polyclonal antiserum was raised in rabbits against a cyanogen bromide-resistant protein extract of mature cysts containing spores of Myxobolus pendula. The antiserum reacted only with proteins associated with extruded polar filaments. Western blot and whole-mount immunohistochemical analyses indicated a conservation of polar filament epitopes between M. pendula and 2 related cnidarians, i.e., the anthozoan, Nematostella vectensis, and the hydrozoan, Hydra vulgaris. This conservation of polar filament epitopes lends further support to a shared affinity between Myxozoa and cnidarians.     

Origin and early diversification of the phylum Cnidaria Verrill: major developments in the analysis of the taxon's Proterozoic–Cambrian history

Diploblastic eumetazoans of the phylum Cnidaria originated during the Neoproterozoic Era, possibly during the Cryogenian Period. The oldest known fossil cnidarians occur in strata of Ediacaran age and consist of polypoid forms that were either nonbiomineralizing or weakly so. The oldest possible anthozoans, including the genus Ramitubus, may be related to tabulate corals and occur in the Doushantuo Lagerstätte (upper Doushantuo Formation, South China), the age of which is poorly constrained (approximately 585 Ma?). Conulariid scyphozoans may first appear as early as 635–577 Ma (Lantian Formation, South China). A definite conulariid, most similar to Palaeozoic species assigned to the genus Paraconularia, occurs in association with the possible scyphozoan, Corumbella werneri, in the latest Ediacaran (c. 543 Ma) Tamengo Formation of Brazil. Basal Cambrian (c. 540 Ma) phosphorites in the upper Kuanchuanpu Formation (South China) yield solitary polyps of the oldest probable anthozoan (Eolympia pediculata), which appears to have been a stem hexacorallian. This same formation contains fossils interpreted by some authors as pentaradial cubozoan polyps; however, both the oldest known cubozoans and the oldest hydrozoans, all medusae, may actually occur in the Cambrian (Series 3, c. 505 Ma) Marjum Formation (Utah, USA). Although these recently published palaeontological data tend to corroborate the hypothesis that Cnidaria has a relatively deep Neoproterozoic history, the timing of major internal branching events remains poorly constrained, with, for example, the results of some molecular clock analyses indicating that the two cnidarian subphyla (Anthozoaria and Medusozoa) may have originated as many as one billion years ago. Further progress towards elucidating the evolution and early fossil record of cnidarians may accrue from: (1) an intensive search for phosphatized soft parts in possible anthozoans from the Ediacaran Doushantuo Formation; (2) an expanded search for Ediacaran conulariids; and (3) additional detailed analyses of the taphonomy and preservation of Ediacaran and Cambrian cnidarians, including possible pentaradial cubozoan polyps from the Fortunian upper Kuanchuanpu Formation.     

Cnidarian taphonomy and affinities of the Ediacara biota

Plaster impressions and sand casts of extant medusae, a chondrophoran, and a pennatulid share basic structural characteristics with fossils in the Upper Proterozoic Ediacara assemblage. Impressions of extant medusae and Proterozoic circular impressions show general similarities in arrangement and position of radial and concentric structures and a central raised boss. However, annular rings and radial grooves are more numerous in the Proterozoic fossils and strongly folded or deformed fossils are rare as compared with impressions of modem medusae. Recent pennatulids yield impressions that are more deformed and irregular than the Proterozoic genus Charniodiscus. The greater frequency of deformation of most simulated fossil medusoids relative to Precambrian circular impressions implies that Proterozoic medu-soids were substantially stiffer than many modern taxa of comparable sizes. Many fossils with abundant circular rings have no constructional counterparts among the extant forms studied here and their medusoid affinities should remain in doubt. The structural simplicity of impressions of Ediacara organisms and extant cnidarians suggests that their mutual similarities may be due to convergence. However, there is no compelling morphological reason to reject the claim that some Proterozoic fossils may share affinities with living cnidarians. □ Taphonomy. Ediacara biota, cnidarians, phylogenetic relationships.     

Insights from diploblasts; the evolution of mesoderm and muscle

The origin of both mesoderm and muscle are central questions in metazoan evolution. The majority of metazoan phyla are triploblasts, possessing three discrete germ layers. Attention has therefore been focused on two outgroups to triploblasts, Cnidaria and Ctenophora. Modern texts describe these taxa as diploblasts, lacking a mesodermal germ layer. However, some members of Medusozoa, one of two subphyla within Cnidaria, possess tissue independent of either the ectoderm or endoderm referred to as the entocodon. Furthermore, members of both Cnidaria and Ctenophora have been described as possessing striated muscle, a mesodermal derivative. While it is widely accepted that the ancestor of Eumetazoa was diploblastic, homology of the entocodon and mesoderm as well as striated muscle within Eumetazoa has been suggested. This implies a potential triploblastic ancestor of Eumetazoa possessing striated muscle. In the following review, I examine the evidence for homology of both muscle and mesoderm. Current data support a diploblastic ancestor of cnidarians, ctenophores, and triploblasts lacking striated muscle.     

Symmetry of priapulids (Priapulida). 1. Symmetry of adults

Priapulids possess a radial symmetry that is remarkably reflected in both external morphology and internal anatomy. It results in the appearance of 25-radial (a number divisible by five) symmetry summarized as a combination of nonaradial, octaradial, and octaradial (9+8+8) symmetries of scalids. The radial symmetry is a secondary appearance considered as an evolutionary adaptation to a lifestyle within the three-dimensional environment of bottom sediment. The eight anteriormost, or primary, scalids retain their particular position because of their innervation directly from the circumpharyngeal brain. As a result of a combination of the octaradial symmetry of primary scalids, pentaradial symmetry of teeth, and the 25-radial symmetry of scalids, the initial bilateral symmetry remains characterized by the single sagittal plane.     

Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances

A striking aspect of flowering plant (angiosperm) diversity is variation in flower symmetry. From an ancestral form of radial symmetry (polysymmetry, actinomorphy), multiple evolutionary transitions have contributed to instances of non-radial forms, including bilateral symmetry (monosymmetry, zygomorphy) and asymmetry. Advances in flowering plant molecular phylogenetic research and studies of character evolution as well as detailed flower developmental genetic studies in a few model species (e.g. Antirrhinum majus, snapdragon) have provided a foundation for deep insights into flower symmetry evolution. From phylogenetic studies, we have a better understanding of where during flowering plant diversification transitions from radial to bilateral flower symmetry (and back to radial symmetry) have occurred. From developmental studies, we know that a genetic programme largely dependent on the functional action of the CYCLOIDEA gene is necessary for differentiation along the snapdragon dorsoventral flower axis. Bringing these two lines of inquiry together has provided surprising insights into both the parallel recruitment of a CYC-dependent developmental programme during independent transitions to bilateral flower symmetry, and the modifications to this programme in transitions back to radial flower symmetry, during flowering plant evolution.     

Cell adhesion molecules and actin cytoskeleton at immune synapses and kinapses

The immunological synapse is a stable adhesive junction between a polarized immune effector cell and an antigen-bearing cell. Immunological synapses are often observed to have a striking radial symmetry in the plane of contact with a prominent central cluster of antigen receptors surrounded by concentric rings of adhesion molecules and actin-rich projections. There is a striking similarity between the radial zones of the immunological synapse and the dynamic actinomyosin modules employed by migrating cells. Breaking the symmetry of an immunological synapse generates a moving adhesive junction that can be defined as a kinapse, which facilitates signal integration by immune cells while moving over the surface of antigen-presenting cells.     

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.     

Morphology,distribution, and evolution of apical structure of nematocysts in hexacorallia

Cnidae are complex intracellular capsules made by all cnidarians. The most diverse of these capsules are nematocysts, which are made by all members of the phylum; spirocysts and ptychocysts are made only by members of some lineages, and they show less functional and structural diversity. In nematocysts, the apex has been shown to be either a hinged cap (operculum) or three flaps that flex outward during discharge. The operculum is known only from medusozoan nematocysts; flaps are known only from nematocysts of members of the hexacorallian order Actiniaria, although they have been inferred to be characteristic of Anthozoa, the group to which Actiniaria belongs. Using scanning and transmission electron microscopy, we discover a third apical morphology in nematocysts, an apical cap, which we find in all nonactiniarian anthozoans examined. This apical cap is identical structurally to the apical cap of spirocysts, and it resembles the apical structure of ptychocysts, whose apex is documented here for the first time. Additionally, a full survey of nematocysts from all body structures of two actiniarians demonstrates that a particular type of nematocyst, the microbasic p‐mastigophore of the mesenterial filaments, does not have apical flaps. The observed variation does not correspond to conventional categorization of capsule morphology and raises questions about the function and structure of capsules across Cnidaria. Despite some ambiguity in optimization of ancestral states across cnidae, we determine that the apical cap is the plesiomorphic structure for anthozoan cnidae and that apical flaps are a synapomorphy of Actiniaria. At present, the operculum is interpreted as a synapomorphy for Medusozoa, but either it or an apical cap is the ancestral state for nematocysts. J. Morphol. 273:121–136, 2011. © 2011 Wiley Periodicals, Inc.     

Paedomorphosis and heterochrony in the origin and evolution of the class holothuroidea

The role of paedomorphosis as a particular case of heterochrony in the origin and evolution of the class Holothuroidea is analyzed. It is shown that holothurians are characterized by the presence of some paedomorphic characters (reduced skeleton, absence of an axial complex in the shape of a morphologically integrated structure, single gonad with one gonopore). In many members of the subclass Holothuriacea, sclerites of the body wall are arranged in two layers. Sclerites of the deeper layer develop as a perforated plate and correspond to the skeletal elements forming in other echinoderms the body skeleton, for example, the test of sea urchins. Sclerites of the superficial layer frequently look like various tables, develop like spines of other echinoderm classes, in particular, juvenile tetraradiate spines of sea urchins, and correspond to spines of other classes of Echinodermata. Ontogenetic changes at the stage of five first tentacles resulted in interruption at an early stage of the development with the catastrophic metamorphosis, which is typical for other Eleutherozoa. The ontogeny of holothurians acquired the evolutive (gradual) character; the adult body began to develop on the basis of the larval body and larval tissues were partially included in the body of adult holothurians. As a result, the place and developmental pattern of the radial complex of organs changed and heterochrony in the development of characters concerned with different coordination chains intensified; therefore, the modern body plan of holothurians was formed. The processes of paedomorphosis and heterochrony played an important role not only in the origin and formation of the class Holothuroidea, but also during its evolution. Paedomorphic processes became rather important in the evolution of the order Synaptida. Paedomorphic features are particularly prominent in the structure of small interstitial forms. In some holothurians, the paedomorphosis resulted in the change in relationships between symmetry planes. The bilateral plane of symmetry of these holothurians coincide with the plane of symmetry 2–1–2, which is positioned in the majority of holothurians at about 72° to the bilateral plane. Independently, but frequently in parallel, the intestinal loop disappeared, so that the gut became straight and suspended on mediodorsal mesentery almost throughout its extent. The combination of these processes in holothurians of the order Synaptida resulted in the formation of almost complete pentaradially bilateral symmetry.     

Cytomorphological characteristics of Polypodium hydriforme and problems of myxozoan and cnidarian phylogeny

The present review analyses cytomorphological characters of the parasitic cnidarian Polypodium hydriforme, discriminating between those of bilateral (triploblastic) animals, common characters shared with the Myxozoa, and the unique characters of this species. Phylogenetic position of the group of parasitic cnidarians and of the class Polypodiozoa is discussed. A conclusion is made that the cytomorphological characters as well as 18S rDNA analysis of P. hydriforme and Myxozoa justify establishment of a new taxonomic group (a clade) of parasitic cnidarians (Endocnidozoa) uniting Polypodiozoa and Myxozoa (Zrzavy, Hypsa, 2003). The unique characters of P. hydriforme suggest that the phylum Cnidaria is more diverse than commonly supposed, and that P. hydriforme is not an aberrant cnidarian species but a relic organism, which might originally belong to the cnidarian class Polypodiozoa, which underwent reduction in the course of adaptation to parasitism.     

Gravity influences the position of the dorsoventral axis in medaka fish embryos (Oryzias latipes)

To determine whether gravity influences the plane of bilateral symmetry in medaka embryos, zygotes were placed with their animal-vegetal axis orientated vertically and with their vegetal pole elevated. Then, at regular intervals during the first cell cycle, the zygotes were tilted 90° for about 10 min and subsequently returned to their original orientation. In embryos tilted during the first half of the first cell cycle, the embryonic shield formed on the side that had been lowermost when the zygote was tilted. In embryos that were tilted twice, first in one direction and then in the opposite direction, the embryonic shield formed on the side that was lowermost the first time. When zygotes were centrifuged at 5 g , the embryonic shield formed on the outwardly radial (centrifugal) side of the embryo. The orientation of the array of parallel microtubules in the vegetal pole region was also influenced by tilting or centrifuging zygotes. No correlation was found between the positions of the polar body and the micropyle and the plane of bilateral symmetry. It was concluded that gravity influences both the plane of bilateral symmetry and the orientation of microtubules in the vegetal pole region of medaka embryos.     

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.     

Origins of radial symmetry identified in an echinoderm during adult development and the inferred axes of ancestral bilateral symmetry

How the radial body plan of echinoderms is related to the bilateral body plan of their deuterostome relatives, the hemichordates and the chordates, has been a long-standing problem. Now, using direct development in a sea urchin, I show that the first radially arranged structures, the five primary podia, form from a dorsal and a ventral hydrocoele at the oral end of the archenteron. There is a bilateral plane of symmetry through the podia, the mouth, the archenteron and the blastopore. This adult bilateral plane is thus homologous with the bilateral plane of bilateral metazoans and a relationship between the radial and bilateral body plans is identified. I conclude that echinoderms retain and use the bilateral patterning genes of the common deuterostome ancestor. Homologies with the early echinoderms of the Cambrian era and between the dorsal hydrocoele, the chordate notochord and the proboscis coelom of hemichordates become evident.