Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences

SUMMARY Insight into the origin and early evolution of the animal phyla requires an understanding of how animal groups are related to one another. Thus, we set out to explore animal phylogeny by analyzing with maximum parsimony 138 morphological characters from 40 metazoan groups, and 304 18S rDNA sequences, both separately and together. Both types of data agree that arthropods are not closely related to annelids: the former group with nematodes and other molting animals (Ecdysozoa), and the latter group with molluscs and other taxa with spiral cleavage. Furthermore, neither brachiopods nor chaetognaths group with deuterostomes; brachiopods are allied with the molluscs and annelids (Lophotrochozoa), whereas chaetognaths are allied with the ecdysozoans. The major discordance between the two types of data concerns the rooting of the bilaterians, and the bilaterian sister-taxon. Morphology suggests that the root is between deuterostomes and protostomes, with ctenophores the bilaterian sister-group, whereas 18S rDNA suggests that the root is within the Lophotrochozoa with acoel flatworms and gnathostomulids as basal bilaterians, and with cnidarians the bilaterian sister-group. We suggest that this basal position of acoels and gnathostomulids is artifactal because for 1000 replicate phylogenetic analyses with one random sequence as outgroup, the majority root with an acoel flatworm or gnathostomulid as the basal ingroup lineage. When these problematic taxa are eliminated from the matrix, the combined analysis suggests that the root lies between the deuterostomes and protostomes, and Ctenophora is the bilaterian sister-group. We suggest that because chaetognaths and lophophorates, taxa traditionally allied with deuterostomes, occupy basal positions within their respective protostomian clades, deuterostomy most likely represents a suite of characters plesiomorphic for bilaterians.     

Biology of the Hyolitha

Hyoliths are Paleozoic fossils that have a calcareous exoskeleton consisting of an elongate, usually bilaterally symmetrical cone, a close fitting operculum, and a pair of curved appendages. Their skeletal ultrastructure resembles the crossed-lamellar shell layers of some molluscs. Several specimens from the Ordovician of France and the Cambrian of Antarctica have parts of the gut preserved by infilling matrix, showing that both mouth ad anus were located near the cone aperture. Muscle scars in other hyolith shells indicate that the animal had a series of dorsoventral and longitudinal, or longitudinal and circular muscles, which operated through a hydrostatic skeleton to protract and retract the head, to open and close the operculum, and to move the appendages. Although the shell form and skeletal ultra-structure of hyoliths are of a molluscan type, the muscle insertions suggest that the hyolith cone is not homologous with the dorsal exoskeleton of primitive molluscs. Hyoliths probably constitute a small extinct branch of phylum size, related to the Mollusca and the Sipunculoidea. All three groups may have had common ancestors in the late Precambrian.     

The Essential Role of "Minor" Phyla in Molecular Studies of Animal Evolution

SYNOPSIS. Molecular studies have revealed many new hypothesesof metazoan evolution in recent years. Previously, using morphologicalmethods, it was difficult to relate "minor" animal groups representingmicroscopic metazoans to larger, more well known groups suchas arthropods, molluscs, and annelids. Molecular studies suggestthat acanthocephalans evolved from rotifers, that priapulidsshare common ancestry with all other molting animals (Ecdysozoa),and that flatworms, gnathostomulids and rotifers form a sistergroup to the remaining non-molting protostomes (Lophotrochozoa),together forming Spiralia. The lophophorate phyla (phoronids,brachiopods and bryozoans) appear as protostomes, allied withannelids and molluscs rather than with deuterostomes. Thesefindings present a very different view of metazoan evolution,and clearly show that small and simple animals do not necessarilyrepresent ancestral or primitive taxa.     

Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion

The embryology of sipunculans, entoprocts, nemertines, platyhelminths (excluding acoelomorphs), rotifers, ectoprocts, phoronids, brachiopods, echinoderms and enteropneusts is reviewed with special emphasis on cell-lineage and differentiation of ectodermal structures. A group Spiralia comprising the four first-mentioned phyla plus annelids and molluscs seems well defined through the presence of spiral cleavage with early blastomere specification, prototroch with characteristic cell-lineage, cerebral ganglia developing from cells of the first micromere quartet (i.e., the episphere) and a ventral nervous system developing from the hyposphere. The planktotrophic trochophore was probably the larval type of the ancestor of this group. Another group comprising phoronids, brachiopods, echinoderms and enteropneusts appears equally well delimited. It is characterized by radial cleavage with late blastomere specification, possibly by the presence of a neotroch consisting of monociliate cells, by the absence of cerebral ganglia and of a well-defined brain and paired longitudinal nerve cords developing in connection with the blastopore, and by coelomic organization. Its ancestral larval type was probably a dipleurula. Several characters link rotifers with the spiralians, although they do not show the spiral pattern in the cleavage. Ectoprocts are still a problematic group, but some characters indicate spiralian affinities.     

Cambrian Onychophora or Xenusians

The Cambrian xenusians have certain similarities to modern onychophorans and tardigrades, and it is tempting to suggest a relationship to one or the other of them. However, similarities are often on a fairly general level. For instance, the three groups all shed their cuticle, but they leave it in three different ways: through a ventral split, through a dorsal split, and through the anterior opening, respectively. Considering also all other characters, we are left with a complicated mosaic character pattern that is indeed difficult to interpret. In addition, the fossils show a great diversity, and there is disagreement on how to interpret some features of them. It seems premature to interpret xenusians as close relatives of any extant group. They may or may not be related: we should also remember the plain fact that an overwhelming majority of characters in organisms have evolved more than once.     

Phylogenetic position of phylum Nemertini, inferred from 18S rRNA sequences: molecular data as a test of morphological character homology.

Partial 18S rRNA sequence of the nemertine Cerebratulus lacteus was obtained and compared with those of coelomate metazoans and acoelomate platyhelminths to test whether nemertines share a most recent common ancestor with the platyhelminths, as traditionally has been implied, or whether nemertines lie within a protostome coelomate clade, as suggested by more recent morphological analyses. Maximum-parsimony analysis supports the inclusion of the nemertine within a protostome-coelomate clade that falls within a more inclusive coelomate clade. Bootstrap analysis indicates strong support for a monophyletic Coelomata composed of a deuterostome and protostome-coelomate clade. Support for a monophyletic protostome Coelomata is weak. Inference by distance analysis is consistent with that of maximum parsimony. Analysis of down-weighted paired sites by maximum parsimony reveals variation in topology only within the protostome-coelomate clade. The relationships among the protostome coelomates cannot be reliably inferred from the partial sequences, suggesting that coelomate protostomes diversified rapidly. Results with evolutionary parsimony are consistent with the inclusion of the nemertine in a coelomate clade. The molecular inference corroborates recent morphological character analyses that reveal no synapomorphies of nemertines and flatworms but instead suggest that the circulatory system and rhynchocoel of nemertines are homologous to coelomic cavities of protostome coelomates, thus supporting the corresponding hypothesis that nemertines belong within a protostome-coelomate clade. The sequence data provide an independent test of morphological character homology.     

Early Cambrian molluscs from Sierra de Córdoba (Spain)

Lower Cambrian helcionelloid molluscs are described from the Pedroche Formation in Sierra de Córdoba, southern Spain. The molluscan fauna occurs together with abundant and diverse Small Shelly Fossils (SSF) in limestone units and limestone nodules within terrigenous units. The molluscs are assigned to three new genera and six new species. Three species are previously known from North Siberia and one occurs in Australia, Altai-Sayan Fold Belt, Siberia, Central Asia, China and eastern Germany. The molluscs and other Small Shelly Fossils indicate close palaeogeographic links to Siberia and other continental blocks during the Early Cambrian.     

Ecological innovations in the Cambrian and the origins of the crown group phyla

Simulation studies of the early origins of the modern phyla in the fossil record, and the rapid diversification that led to them, show that these are inevitable outcomes of rapid and long-lasting radiations. Recent advances in Cambrian stratigraphy have revealed a more precise picture of the early bilaterian radiation taking place during the earliest Terreneuvian Series, although several ambiguities remain. The early period is dominated by various tubes and a moderately diverse trace fossil record, with the classical ‘Tommotian’ small shelly biota beginning to appear some millions of years after the base of the Cambrian at ca 541 Ma. The body fossil record of the earliest period contains a few representatives of known groups, but most of the record is of uncertain affinity. Early trace fossils can be assigned to ecdysozoans, but deuterostome and even spiralian trace and body fossils are less clearly represented. One way of explaining the relative lack of clear spiralian fossils until about 536 Ma is to assign the various lowest Cambrian tubes to various stem-group lophotrochozoans, with the implication that the groundplan of the lophotrochozoans included a U-shaped gut and a sessile habit. The implication of this view would be that the vagrant lifestyle of annelids, nemerteans and molluscs would be independently derived from such a sessile ancestor, with potentially important implications for the homology of their sensory and nervous systems.     

A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors

Aplacophorans have long been argued to be basal molluscs. We present a molecular phylogeny, including the aplacophorans Neomeniomorpha (Solenogastres) and Chaetodermomorpha (Caudofoveata), which recovered instead the clade Aculifera (Aplacophora + Polyplacophora). Our relaxed Bayesian molecular clock estimates an Early Ordovician appearance of the aculiferan crown group consistent with the presence of chiton-like molluscs with seven or eight dorsal shell plates by the Late Cambrian (approx. 501-490 Ma). Molecular, embryological and palaeontological data indicate that aplacophorans, as well as chitons, evolved from a paraphyletic assemblage of chiton-like ancestors. The recovery of cephalopods as a sister group to aculiferans suggests that the plesiomorphic condition in molluscs might be a morphology similar to that found in monoplacophorans.     

Anabarella australis (Mollusca, Helcionelloida) from the Lower Cambrian of Greenland

The Early Cambrian helcionelloid mollusc Anabarella australis is described from North-East Greenland, representing the second occurrence of the species outside of Australia. Other Australian molluscs of this age are known from many localities including North China, Siberia, Altai, Transbaikalia, southern Kazakhstan, Mongolia, eastern Germany and Spain. These records, supported now by A. australis, demonstrate the close proximity of continents in the Early Cambrian.     

Some aspects of spiralian development

Nielsen, C. 2010. Some aspects of spiralian development. —Acta Zoologica (Stockholm) 91 : 20–28 Spiralian development is not only a characteristic early cleavage pattern, with shifting orientations of the cleavage planes, but also highly conserved cell lineages, where the origin of several organs can be traced back to identifiable cells in the lineage. These patterns are well documented in annelids, molluscs, nemertines, and platyhelminths and are considered ancestral of a bilaterian clade including these phyla. Spiral cleavage has not been documented in ecdysozoans, and no trace of the spiral development pattern is seen in phoronids and brachiopods. Origin of the spatial organization in spiralian embryos is puzzling, but much of the information appears to be encoded in the developing oocyte. Fertilization and “pseudofertilization” apparently provides the information defining the secondary, anterior‐posterior body axis in many species. The central nervous system consists of three components: an apical organ, derived from the apical blastomeres 1a¹¹¹‐1d¹¹¹, which degenerates before or at metamorphosis; the cerebral ganglia derived from other blastomeres of the first micromere quartet and retained in the adult as a preoral part of the brain; and the originally circumblastoporal nerve cord, which has become differentiated into a perioral part of the brain, the paired or secondarily fused ventral nerve cords, and a small perianal nerve ring.     

The dawn of bilaterian animals: the case of acoelomorph flatworms

The origin of the bilaterian metazoans from radial ancestors is one of the biggest puzzles in animal evolution. A way to solve it is to identify the nature and main features of the last common ancestor of the bilaterians (LCB). Recent progress in molecular phylogeny has shown that many platyhelminth flatworms, regarded for a long time as basal bilaterians, now belong to the lophotrochozoan protostomates. In contrast, the LCB is now considered a complex organism bearing several features of modern bilaterians. Here we discuss an alternative view, in which acoelomorph (Acoela + Nemertodermatida) flatworms, which do not belong to the Platyhelminthes, represent the earliest extant bilaterian clade. Sequences from ribosomal and other nuclear genes, Hox cluster genes, and reinterpretation of some morphological features strongly support the basal position of acoelomorphs arguing against a complex LCB. This reconstruction backs the old planuloid-acoeloid hypothesis and may help our understanding of the evolution of body axes, Hox genes and the Cambrian explosion.     

The origin of crustaceans: new evidence from the Early Cambrian of China.

One of the smallest arthropods recently discovered in the Early Cambrian Maotianshan Shale Lagerstätte is described. Ercaia gen. nov. has an untagmatized trunk bearing serially repeated biramous appendages (long and segmented endopods and flap-like exopods), a head with an acron bearing stalked lateral eyes and a sclerite and two pairs of antennae. The position of this 520 million-year-old tiny arthropod within the Crustacea is supported by several anatomical features: (i) a head with five pairs of appendages including two pairs of antennae, (ii) highly specialized antennae (large setose fans with a possible function in feeding), and (iii) specialized last trunk appendages (segmented pediform structures fringed with setae). The segmentation pattern of Ercaia (5 head and 13 trunk) is close to that of Maxillopoda but lacks the trunk tagmosis of modern representatives of the group. Ercaia is interpreted as a possible derivative of the stem group Crustacea. Ercaia is likely to have occupied an ecological niche similar to those of some Recent meiobenthic organisms (e.g. copepods living in association with sediment). This new fossil evidence supports the remote ancestry of crustaceans well before the Late Cambrian and shows, along with other fossil data (mainly Early Cambrian in China), that a variety of body plans already coexisted among the primitive crustacean stock.     

Wandel der Vorstellungen von der Frühevolution der Mollusken,besonders der Gastropoda und Cephalopoda

The ancestors of the molluscs are still unknown. Arguments in favour of flatworm-relationship are just as valid as those proposing segmented annelid-like worms as their closest relatives. The earliest molluscs lived before the onset of the Cambrian; but only at the end of this period the now existing classes of conchifers made their first appearance. Early and Middle Cambrian molluscan fossils are problematic. The hyoliths, for example, show relations to such fossils asSalterella andVolborthella, while closest living relatives can be found among tube-building annelids. Scars produced by tissue attached to the shell are of no use in the reconstruction of molluscan phylogeny, but a very useful tool in the analysis of the function regarding the body in interaction with its shell. The ontogenesis of the shell and muscles attached to it in recentFissurella (archaeogastropod) is presented as an example. Well known ontogenies in recent molluscs can aid to the reconstruction of fossils, demonstrated by some fossil gastropods. The interaction of soft and hard tissues, the function and structure of the shell of recent molluscs enables us to interpret the fossil forms, as for example the Lower Devonian coleoid cephalopods from the Hunsrück Schiefer. Reconstruction of the course of evolution is only possible, if information on living molluscs is integrated into historical data provided by the fossils.     

寒武纪早期疑难生物类群阿纳巴管(Anabarites)亲缘性的探讨

阿纳巴管为生活于寒武纪早期、具三射对称管栖疑难生物。文中通过对采自陕西南部宁强下寒武统宽川铺组阿纳巴管壳体SEM和岩石薄片的观察,并以对称性和矿物组成作为线索对阿纳巴管的系统学位置和生物属性开展了探索。通过对称性对比研究和骨骼矿物组成的研究,将阿纳巴管解释为珊瑚虫纲古老干支类群的化石代表,为现生六射珊瑚的祖先类群。根据阿纳巴管个体发育过程对称性的演变所提供的线索进一步认为以六射及其倍数对称为特征的现代六射珊瑚可能经过三射对称中间阶段,起源于圆形辐射对称的祖先。阿纳巴管为由圆形经三射向六射转变这一中间阶段的化石代表。此外,还对阿纳巴管的成岩模式以及生活方式开展了探索性研究。     

Homologous shell microstructures in Cambrian hyoliths and molluscs

Hyoliths were among the earliest biomineralizing metazoans in Palaeozoic marine environments. They have been known for two centuries and widely assigned to lophotrochozoans. However, their origin and relationships with modern lophotrochozoan clades have been a longstanding palaeontological controversy. Here, we provide broad microstructural data from hyolith conchs and opercula from the lower Cambrian Xinji Formation of North China, including two hyolithid genera and four orthothecid genera as well as unidentified opercula. Results show that most hyolith conchs contain a distinct aragonitic lamellar layer that is composed of foliated aragonite, except in the orthothecid New taxon 1 that has a crossed foliated lamellar microstructure. Opercula are mostly composed of foliated aragonite and occasionally foliated calcite. These blade or lath‐like microstructural fabrics coincide well with biomineralization of Cambrian molluscs rather than lophophorates, as exemplified by the Cambrian members of the tommotiid‐brachiopod linage. Accordingly, we propose that hyoliths and molluscs might have inherited their biomineralized skeletons from a non‐mineralized or weakly mineralized common ancestor rather than as a result of convergence. Consequently, from the view of biomineralization, the homologous shell microstructures in Cambrian hyoliths and molluscs strongly strengthen the phylogenetic links between the two groups.     

To Be or Not to Be a Flatworm: The Acoel Controversy

Since first described, acoels were considered members of the flatworms (Platyhelminthes). However, no clear synapomorphies among the three large flatworm taxa - the Catenulida, the Acoelomorpha and the Rhabditophora - have been characterized to date. Molecular phylogenies, on the other hand, commonly positioned acoels separate from other flatworms. Accordingly, our own multi-locus phylogenetic analysis using 43 genes and 23 animal species places the acoel flatworm Isodiametra pulchra at the base of all Bilateria, distant from other flatworms. By contrast, novel data on the distribution and proliferation of stem cells and the specific mode of epidermal replacement constitute a strong synapomorphy for the Acoela plus the major group of flatworms, the Rhabditophora. The expression of a piwi-like gene not only in gonadal, but also in adult somatic stem cells is another unique feature among bilaterians. These two independent stem-cell-related characters put the Acoela into the Platyhelminthes-Lophotrochozoa clade and account for the most parsimonious evolutionary explanation of epidermal cell renewal in the Bilateria. Most available multigene analyses produce conflicting results regarding the position of the acoels in the tree of life. Given these phylogenomic conflicts and the contradiction of developmental and morphological data with phylogenomic results, the monophyly of the phylum Platyhelminthes and the position of the Acoela remain unresolved. By these data, both the inclusion of Acoela within Platyhelminthes, and their separation from flatworms as basal bilaterians are well-supported alternatives.     

An early Ordovician patelliform gastropod, Palaelophacmaea, reinterpreted as a coelenterate

Yochelson, Ellis L. & Stanley, George D., Jr. 1981 12 15: An early Ordovician patelliform gastropod, Palaelophacmaea , reinterpreted as a coelenterate. Lethaia , Vol. 15, pp. 323–330. Oslo. ISSN W24–1164.
The fossil Palaelophacmaea criola Donaldson, from the early Ordovician Stonehenge Formation of central Pennsylvania, was described as a patelliform gastropod. A reinterpretation of the type lot and study of a few additional specimens provide the basis for an alternative placement. Palaelophacmaea is here assigned to the Hydrozoa, as a possible chondrophore. It has an exceptionally thin shell or test and concentric but irregular corrugations. Cambrian univalve genera having a more or less circular outline that are currently assigned to the Gastropoda or Monoplacophora should be reexamined to see whether they have the features of fossil chondrophore coelenterates rather than those of molluscs. The late Cambrian Palaeoacmaea Hall & Whitfield is removed from the monoplacophoran Mollusca and left unassigned as to phylum. We judge that at least some early Cambrian species of Scenella are probably coelenterate remains. * Early Ordovician , Palaelophacmaea, Gastropoda, Monoplacophora, Hydrozoa .     

Origin and evolution of the panarthropod head – A palaeobiological and developmental perspective

The panarthropod head represents a complex body region that has evolved through the integration and functional specialization of the anterior appendage-bearing segments. Advances in the developmental biology of diverse extant organisms have led to a substantial clarity regarding the relationships of segmental homology between Onychophora (velvet worms), Tardigrada (water bears), and Euarthropoda (e.g. arachnids, myriapods, crustaceans, hexapods). The improved understanding of the segmental organization in panarthropods offers a novel perspective for interpreting the ubiquitous Cambrian fossil record of these successful animals. A combined palaeobiological and developmental approach to the study of the panarthropod head through deep time leads us to propose a consensus hypothesis for the intricate evolutionary history of this important tagma. The contribution of exceptionally preserved brains in Cambrian fossils – together with the recognition of segmentally informative morphological characters – illuminate the polarity for major anatomical features. The euarthropod stem-lineage provides a detailed view of the step-wise acquisition of critical characters, including the origin of a multiappendicular head formed by the fusion of several segments, and the transformation of the ancestral protocerebral limb pair into the labrum, following the postero-ventral migration of the mouth opening. Stem-group onychophorans demonstrate an independent ventral migration of the mouth and development of a multisegmented head, as well as the differentiation of the deutocerebral limbs as expressed in extant representatives. The anterior organization of crown-group Tardigrada retains several ancestral features, such as an anterior-facing mouth and one-segmented head. The proposed model aims to clarify contentious issues on the evolution of the panarthropod head, and lays the foundation from which to further address this complex subject in the future.     

Molecular data indicate the protostome affinity of brachiopods

Although the phylogenetic position of brachiopods has always been subject to debate, many authors place them as a sister group to deuterostomes on the basis of morphological and developmental characters. However, molecular phylogeny consistently places them among protostomes. More precisely, brachiopods are predicted to branch inside the lophotrochozoan assemblage, together with annelids, molluscs, nemerteans, flatworms, and others. That result has been criticized on the basis of (1) prior knowledge of brachiopod morphology and (2) the known limitations of molecular phylogenies. Here I review recent data of molecular origin, particularly those displaying qualitative properties close to those of morphological characters. The complement of Hox genes present in all metazoa tested to date has proved to be a powerful tool for broad phylogenetic reconstruction. The mitochondrial genome also provides qualitative characters, showing discrete events of gene rearrangements. After discussing the data and the way they should be interpreted in the perspective of several hypotheses for metazoan phylogeny, I conclude that they argue strongly in favor of the protostome (and lophotrochozoan) affinity of the brachiopods. There is therefore a need for a reinterpretation of brachiopod morphological and developmental characters. I also identify some research axes on brachiopod morphology.