Defining phyla: evolutionary pathways to metazoan body plans

SUMMARY Phyla are defined by two sets of criteria, one morphological and the other historical. Molecular evidence permits the grouping of animals into clades and suggests that some groups widely recognized as phyla are paraphyletic, while some may be polyphyletic; the phyletic status of crown phyla is tabulated. Four recent evolutionary scenarios for the origins of metazoan phyla and of supraphyletic clades are assessed in the light of a molecular phylogeny: the trochaea hypothesis of Nielsen; the clonal hypothesis of Dewel; the set-aside cell hypothesis of Davidson et al.; and a benthic hypothesis suggested by the fossil record. It is concluded that a benthic radiation of animals could have supplied the ancestral lineages of all but a few phyla, is consistent with molecular evidence, accords well with fossil evidence, and accounts for some of the difficulties in phylogenetic analyses of phyla based on morphological criteria.     

Determination of whole prokaryotic phylogeny by the development of a random extraction method

The construction of accurate prokaryotic phylogeny is important not only in the field of evolutionary biology, but also in microbiology and pathology. However, in constructing a phylogenetic tree to trace prokaryotic evolution, the phylogenetic relationship is often changed by the choice of species. For the estimation of the accurate lineage of prokaryotes, a new method, named the "random extraction method", was developed. In this method, 16S rRNA sequence data were randomly extracted 1000 times from each closely-related taxa such as seven phyla of Eubacteria and one domain of Archaea and phylogenetic trees were constructed by the data to clarify the relationship of those groups. Next, the tree topology was counted and the most supported tree topology was found as the most plausible phylogenetic tree. To evaluate the reliability of each node, we developed the "Branching rate" (BR) and calculated for every tree. And also, computational simulation analysis was carried out to confirm these methods. On the assumption that the root of life is between Archaea and Eubacteria, the obtained phylogenetic relationships of phyla are the following. At first, Archaea (Euryarchaeota, Crenarchaeota and Korarchaeota) diverged, and Thermotogales, Cyanobacteria and Chlamydiales diverged in this order, then Firmicutes (Actinobacteria and Bacillus/Clostridium group cluster) and Proteobacteria (alpha and beta/gamma cluster) diverged. In addition, it was shown by the BR that the position of the node of Firmicutes Actinobacteria and Firmicutes Bacillus/Clostridium was changeable for each extraction. Therefore, it was suggested that the differences among the phylogenetic trees of prokaryotes were caused by the influence of these phyla.     

The triradiate sucking pharynx in animal phylogeny

Independent sucking/swallowing pharynges, as found in members of at least ten animal phyla, are pharynges that are opened by muscles that are not attached to the outer body wall. Their musculature is derived from either mesoderm or ectoderm, the latter taking the form of a myoepithelium. I review results of previous work on the morphology of independent sucking/swallowing pharynges among invertebrates and provide new information on the ultrastructure of the pharynx of the cyclostome bryozoan Crisia eburnea. The various morphologies of this type of pharynx have been used in some phylogenetic considerations, but only the myoepithelial sucking pharynx with a triradiate lumen was considered significant in analyses of relationships between phyla. However, I argue that this shape is the only one that makes an efficient suction pump, and this, together with different orientations of the myoepithelial pharyngeal pump and its phylogenetic distribution, indicates that the triradiate myoepithelial pharynx has evolved convergently in a number of lineages.     

Phylogeny of Proteobacteria and Bacteroidetes from oxic habitats of a tidal flat ecosystem

Bacteria of the phyla Proteobacteria and Bacteroidetes are known to be the most prominent heterotrophic organisms in marine surface waters. In order to investigate the occurrence of these phyla in a coastal environment, the tidal flat ecosystem German Wadden Sea, we analyzed a clone library of PCR-amplified and sequenced 16S rRNA gene fragments and isolated 46 new strains affiliated with these phyla from the water column with various polymers and complex media as substrates. The phylogenetic affiliation of these strains was analyzed on the basis of sequenced 16S rRNA gene fragments. Subsequently, a comprehensive phylogenetic analysis of Proteobacteria and Bacteroidetes including available sequences from oxic habitats of earlier studies of this ecosystem was performed. Sequences of the earlier studies were derived from isolation approaches and from denaturing gradient gel electrophoresis (DGGE) analyses of environmental samples and high dilution steps of MPN (most probable number) cultures. The majority of the 265 sequences included in this analysis affiliated with alpha-Proteobacteria (45.3%), gamma-Proteobacteria (31.7%), and Bacteroidetes (16.2%). Almost 7% belong to the delta-Proteobacteria and several of these clones affiliated with the Myxococcales, a group comprising obligate aerobic organisms. Within the alpha- and gamma-Proteobacteria specific clusters were identified including isolates from high dilution steps of dilution cultures and/or clones from the clone library or DGGE gels, implying a high abundance of some of these organisms. Within the gamma-Proteobacteria a new cluster is proposed, which consists of marine surface-attached organisms. This SAMMIC (Surface Attached Marine MICrobes) cluster comprises only uncultured phylotypes and exhibits a global distribution. Overall, the analysis indicates that Proteobacteria and Bacteroidetes of the Wadden Sea have a surprisingly high diversity, presumably a result of the signature of this ecosystem as a melting pot at the land-sea interface and comprising a great habitat variety.     

Hox clusters and bilaterian phylogeny

A large Hox cluster comprising at least seven genes has evolved by gene duplications in the ancestors of bilaterians. It probably emerged from a mini-cluster of three or four genes that was present before the divergence of cnidarians and bilaterians. The comparison of Hox structural data in bilaterian phyla shows that the genes of the anterior part of the cluster have been more conserved than those of the posterior part. Some specific signature sequences, present in the form of signature residues within the homeodomain or conserved peptides outside the homeodomain, constitute phylogenetic evidence for the monophyly of protostomes and their division into ecdysozoans and lophotrochozoans. These conserved motifs may provide decisive arguments for the phylogenetic position of some enigmatic phyla.     

Metaphylogeny of 82 gene families sheds a new light on chordate evolution

Achieving a better comprehension of the evolution of species has always been an important matter for evolutionary biologists. The deuterostome phylogeny has been described for many years, and three phyla are distinguishable: Echinodermata (including sea stars, sea urchins, etc...), Hemichordata (including acorn worms and pterobranchs), and Chordata (including urochordates, cephalochordates and extant vertebrates). Inside the Chordata phylum, the position of vertebrate species is quite unanimously accepted. Nonetheless, the position of urochordates in regard with vertebrates is still the subject of debate, and has even been suggested by some authors to be a separate phylum from cephalochordates and vertebrates. It was also the case for agnathans species -myxines and hagfish- for which phylogenetic evidence was recently given for a controversial monophyly. This raises the following question: which one of the cephalochordata or urochordata is the sister group of vertebrates and what are their relationships? In the present work, we analyzed 82 protein families presenting homologs between urochordata and other deuterostomes and focused on two points: 1) testing accurately the position of urochordata and cephalochordata phyla in regard with vertebrates as well as chordates monophyly, 2) performing an estimation of the rate of gene loss in the Ciona intestinalis genome. We showed that the urochordate phyla is the vertebrate sister group and that gene loss played a major role in structuring the urochordate genome.     

Characterization of chemoautotrophic bacterial symbionts in a gutless marine worm Oligochaeta, Annelida) by phylogenetic 16S rRNA sequence analysis and in situ hybridization.

The phylogenetic relationships of chemoautotrophic endosymbionts in the gutless marine oligochaete Inanidrilus leukodermatus to chemoautotrophic ecto- and endosymbionts from other host phyla and to free-living bacteria were determined by comparative 16S rRNA sequence analysis. Fluorescent in situ hybridization confirmed that the 16S rRNA sequence obtained from these worms originated from the symbionts. The symbiont sequence is unique to I. leukodermatus. In phylogenetic trees inferred by both distance and parsimony methods, the oligochaete symbiont is peripherally associated with one of two clusters of chemoautotrophic symbionts that belong to the gamma subdivision of the Proteobacteria. The endosymbionts of this oligochaete form a monophyletic group with chemoautotrophic ectosymbionts of a marine nematode. The oligochaete and nematode symbionts are very closely related, although their hosts belong to separate, unrelated animal phyla. Thus, cospeciation between the nematode and oligochaete hosts and their symbionts could not have occurred. Instead, the similar geographic locations and habitats of the hosts may have influenced the establishment of these symbioses.     

Comparative aspects of invertebrate neuropeptides

1. We searched for bioactive peptides, most of which were considered to be neuropeptides, in various animals of several phyla. These peptides were compared with each other and with peptides identified by many other investigators. Consequently, we found that structures of neuropeptides are generally conserved in each phylum. 2. We also found some exceptional interesting aspects. First, there are a number of peptide groups whose members are distributed among several phyla. Second, there are many structural similarities between molluscan and annelidan peptides as if molluscs and annelids were the animals in a phylum. Third, certain toxic peptides of invertebrates are closely related to vertebrate neuropeptides. 3. In addition to the above phylogenetic aspects, we found some other interesting aspects. A wide structural variety of members of a peptide group is generally found in invertebrate species. Invertebrate muscles seem to be generally regulated not only by some or several classical non-peptidic neuromediators but also by various peptidic neuromediators. Peptides containing a D-amino acid residue are not rare.     

THE AGE AND RELATIONSHIPS OF THE MAJOR ANIMAL PHYLA

Given the uncertainties in the fossil record and the paucity of informative morphological characters, there is still considerable uncertainty as to the phylogenetic affinities and times of origins of essentially all of the phyla of animals. A multilocus analysis of amino-acid sequence data for mitochondrial genes suggests that the major triploblast phyla began diverging approximately 630 million years ago. These results support the hypothesis that the so-called Cambrian radiation of animals actually initiated about 100 million years prior to the Cambrian, as the fossil evidence suggests. In addition, phylogenetic analysis supports the monophyly of animals, an early (~900 million years ago) branching off of the cnidarian lineage, the monophyly of deuterostomes and protostomes, and the inclusion of nematodes in the protostome lineage. The results of this study suggest that, with appropriate levels of taxon sampling and a focus on conserved regions of protein-coding sequence, complete mitochondrial genome analysis may be sufficiently powerful to elucidate the genealogical relationships of many of the animal phyla.     

Defining phyla: morphological and molecular clues to metazoan evolution

None of the supraspecific taxonomic categories can be defined objectively. Each taxon should of course be monophyletic, but there is no morphological or molecular character that identifies, for example, the phylum level. This has led some authors to abandon the Linnaean categories, but they appear to be practical "handles" in daily communication. It has been proposed that each phylum exhibits a characteristic Bauplan, but the identification of such "types" have in practice proved difficult or impossible for several phyla. Monophyly of some of the approximately 30 morphology-based phyla has been put in question by molecular studies, but recent reports clearly show that the 18S rRNA molecule, which has been used extensively in phylogenetic analyses, cannot be used alone in identifying phyla (or other higher taxonomic groups). Some higher taxa, for example Chordata, Vertebrata, and Echinodermata, consistently show up as monophyletic in the analyses, whereas molluscan and annelidan subgroups just as consistently are mixed with each other and with a number of other protostomian phyla in varying patterns.     

A major clade of prokaryotes with ancient adaptations to life on land

Evolutionary trees of prokaryotes usually define the known classes and phyla but less often agree on the relationships among those groups. This has been attributed to the effects of horizontal gene transfer, biases in sequence change, and large evolutionary distances. Furthermore, higher level clades of prokaryote phyla rarely are supported by information from ecology and cell biology. Nonetheless, common patterns are beginning to emerge as larger numbers of species are analyzed with sophisticated methods. Here, we show how combined evidence from phylogenetic, cytological, and environmental data support the existence of an evolutionary group that appears to have had a common ancestor on land early in Earth's history and includes two-thirds of known prokaryote species. Members of this terrestrial clade (Terrabacteria), which includes Cyanobacteria, the gram-positive phyla (Actinobacteria and Firmicutes), and two phyla with cell walls that differ structurally from typical gram-positive and gram-negative phyla (Chloroflexi and Deinococcus-Thermus), possess important adaptations such as resistance to environmental hazards (e.g., desiccation, ultraviolet radiation, and high salinity) and oxygenic photosynthesis. Moreover, the unique properties of the cell wall in gram-positive taxa, which likely evolved in response to terrestrial conditions, have contributed toward pathogenicity in many species. These results now leave open the possibility that terrestrial adaptations may have played a larger role in prokaryote evolution than currently understood.     

Group I Introns from Zygomycota: Evolutionary Implications for the Fungal IC1 Intron Subgroup

The origins of fungal group I introns within nuclear small-subunit (nSSU) rDNA are enigmatic. This is partly because they have never been reported in basal fungal phyla (Zygomycota and Chytridiomycota), which are hypothesized to be ancestral to derived phyla (Ascomycota and Basidiomycota). Here we report group I introns from the nSSU rDNA of two zygomycete fungi, Zoophagus insidians (Zoopagales) and Coemansia mojavensis (Kickxellales). Secondary structure analyses predicted that both introns belong to the IC1 subgroup and that they are distantly related to each other, which is also suggested by different insertion sites. Molecular phylogenetic analyses indicated that the IC1 intron of Z. insidians is closely related to the IC1 intron inserted in the LSU rDNA of the basidiomycete fungus Clavicorona taxophila, which strongly suggests interphylum horizontal transfer. The IC1 intron of C. mojavensis has a low phylogenetic affinity to other fungal IC1 introns inserted into site 943 of nSSU rDNA (relative to E. coli 16S rDNA). It is noteworthy that this intron contains a putative ORF containing a His–Cys box motif in the antisense strand, a hallmark for nuclear-encoded homing endonucleases. Overall, molecular phylogenetic analyses do not support the placement of these two introns in basal fungal IC1 intron lineages. This result leads to the suggestion that fungal IC1 introns might have invaded or been transferred laterally after the divergence of the four major fungal phyla. Received: 8 February 2001 / Accepted: 1 November 2001     

Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements

Phylogenetic relationships among the metazoan phyla are the subject of an ongoing controversy. Analysis of mitochondrial gene arrangements is a powerful tool to investigate these relationships; however, its previous application outside of individual animal phyla has been hampered by the lack of informative out-group data. To address this shortcoming, we determined complete mitochondrial DNA sequences for the demosponges Geodia neptuni and Tethya actinia, two representatives of the most basal animal phylum, the Porifera. With sponges as an outgroup, we investigated phylogenetic relationships of nine bilaterian phyla using both breakpoint analysis of global mitochondrial gene arrangements and maximum parsimony analysis of mitochondrial gene adjacencies. Our results provide strong support for a group that includes protostome (but not deuterostome) coelomate, pseudocoelomate, and acoelomate animals, thus clearly rejecting the Coelomata hypothesis. Two other groups of bilaterian animals, Lophotrochozoa and Ambulacraria, are also supported by our analyses. However, due to the remarkable stability of mitochondrial gene arrangements in Deuterostomia and the Ecdysozoa, conclusions on their evolutionary history cannot be drawn.     

Evolutionary relationships among basal fungi (Chytridiomycota and Zygomycota): Insights from molecular phylogenetics

Evolutionary relationships of the two basal fungal phyla Chytridiomycota and Zygomycota are reviewed in light of recent molecular phylogenetic investigation based on rDNA (nSSU, nLSU rDNA), entire mitochondrial genomes, and nuclear protein coding gene sequences (e.g., EF-1alpha, RPB1). Accumulated molecular evidence strongly suggests that the two basal fungal phyla are not monophyletic. For example, the chytridiomycete order Blastocladiales appears to be closely related to the zygomycete order Entomophthorales. Within the Zygomycota, a monophyletic clade, consisting of the Dimargaritales, Harpellales, and Kickxellales, which is characterized by a shared unique septal ultrastructure, was identified. Moreover, evidence for the exclusion of zygomycete orders Amoebidiales and Eccrinales from the Fungi, and their placement at the Animal-Fungi boundary has been clearly documented. Microsporidia, a group of amitochondriate organisms currently under intensive study, is not supported as derived within the Fungi, but a fungal affinity cannot be ruled out. Taking these molecular phylogenetic studies into account, we proposed a hypothetical evolutionary framework of basal fungi.     

Phylogenetic systematics of microorganisms inhabiting thermal environments

Thermal habitats harbor specialized communities of thermophilic microorganisms, primarily prokaryotes. This review considers modern systematics of prokaryotes and the place of thermophilic archaea and bacteria in it. Among the existing hierarchical classifications of prokaryotes, the bulk of attention is given to the one accepted in the current second edition of "Bergey's Manual of Systematic Bacteriology", which is primarily based on 16S rRNA phylogeny and phenotypic properties of the organisms. Analysis of the genomics data shows that they on the whole agree with the 16S rRNA-based system, although revealing the significance of the evolutionary role of lateral transfer, duplication, and loss of genes. According to the classification elaborated in the current edition of "Bergey's Manual", the prokaryotes currently culturable under laboratory conditions are distributed among 26 phyla, two of which belong to the domain Archaea and 24 to the domain Bacteria. Six phyla contain exclusively thermophiles, and eleven phyla contain thermophiles along with mesophiles, thermophiles being usually separated phylogenetically and representing high-level taxa (classes, orders). In light of the data on the topology of the 16S rRNA-based phylogenetic tree and some other data, this review discusses the probable hyperthermophilic nature of the universal common ancestor.     

Parasites within the new phylogeny of eukaryotes

In the past few years, molecular phylogenetic and cladistic analyses of the interrelationships of the living phyla have resulted in a radical reorganization of eukaryote groups. This reorganization has significance for parasitologists, in that it places as sister taxa some of the more speciose and highly parasitic phyla (nematodes and insects), reorganizes what is now recognized as paraphyletic sets of 'wormy taxa' as the Aschelmintha, and draws numerous bridges between different realms (plants, fungi and animals). This review attempts to explore the role of parasites within the phylogeny of eukaryotes. Extant described parasitic organisms are less common among the eukaryotes than is commonly admitted in the literature.     

Organogenesis in the budding process of the freshwater bryozoan Cristatella mucedo Cuvier, 1798 (bryozoa,phylactolaemata)

The phylogenetic position of bryozoans has been disputed for decades, and molecular phylogenetic analyzes have not unequivocally clarified their position within the Bilateria. As probably the most basal bryozoans, Phylactolaemata is the most promising taxon for large‐scale phylogenetic comparisons. These comparisons require extending the morphological and developmental data by investigating different phylactolaemate species to identify basal characters and resolve in‐group phylogeny. Accordingly, we analyzed the bud development and the organogenesis of the freshwater bryozoan Cristatella mucedo, with special focus on the formation of the digestive tract and differentiation of the coelomic compartments. Most parts of the digestive tract are formed as an outpocketing at the future anal side growing towards the mouth area. The ganglion is formed by an invagination between the anlagen of the mouth and anus. The lophophoral arms develop as paired lateral protrusions into the lumen of the bud and are temporarily connected by a median, thin bridge. All coelomic compartments are confluent during their development and also in the adult. The epistome coelom develops by fusion of two peritoneal infolds between the gut loop and overgrows the ganglion medially. The coelomic ring canal on the oral side develops by two lateral ingrowths and supplies the oral tentacles. On the forked canal, supplying the innermost row of tentacles above the epistome, a bladder‐shaped swelling, probably with excretory function, is present in some adults. It remains difficult to draw comparisons to other phyla because only few studies have dealt with budding of potentially related taxa in more detail. Nonetheless, our results show that comparative organogenesis can contribute to phylactolaemate systematics and, when more data are available, possibly to that of other bryozoan classes and bilaterian phyla. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.