The mitochondrial genome of Phoronis architecta--comparisons demonstrate that phoronids are lophotrochozoan protostomes

The proper reconstruction of the relationships among the animal phyla is central to interpreting patterns of animal evolution from the genomic level to the morphological level. This is true not only of the more speciose phyla but also of smaller groups. We report here the nearly complete DNA sequence of the mitochondrial genome of the phoronid Phoronis architecta, which has a gene arrangement remarkably similar to that of a protostome animal, the chiton Katharina tunicata. Evolutionary analysis of both gene arrangements and inferred amino acid sequences of these taxa, along with those of three brachiopods and other diverse animals, strongly supports the hypothesis that lophophorates are part of the large group that includes mollusks and annelids-i.e., the Lophotrochozoa-and solidly refutes the alternative of their being deuterostomes.     

Evo-devo: variations on ancestral themes

Most animals evolved from a common ancestor, Urbilateria, which already had in place the developmental genetic networks for shaping body plans. Comparative genomics has revealed rather unexpectedly that many of the genes present in bilaterian animal ancestors were lost by individual phyla during evolution. Reconstruction of the archetypal developmental genomic tool-kit present in Urbilateria will help to elucidate the contribution of gene loss and developmental constraints to the evolution of animal body plans.     

Chordate evolution in a new light

Gene expression studies in embryos often provide insights into evolutionary relationships across phyla. In this issue of Cell, Lowe et al. examine the patterning of the bilaterian nervous system by studying gene expression in a hemichordate, the acorn worm. Although these animals have an unstructured nervous system, they show surprisingly conserved gene expression domains, shedding new light on the evolution of the central nervous system and the phylogenetic placement of chordates.     

A bayesian analysis of metazoan mitochondrial genome arrangements

Genome arrangements are a potentially powerful source of information to infer evolutionary relationships among distantly related taxa. Mitochondrial genome arrangements may be especially informative about metazoan evolutionary relationships because (1) nearly all animals have the same set of definitively homologous mitochondrial genes, (2) mitochondrial genome rearrangement events are rare relative to changes in sequences, and (3) the number of possible mitochondrial genome arrangements is huge, making convergent evolution of genome arrangements appear highly unlikely. In previous studies, phylogenetic evidence in genome arrangement data is nearly always used in a qualitative fashion-the support in favor of clades with similar or identical genome arrangements is considered to be quite strong, but is not quantified. The purpose of this article is to quantify the uncertainty among the relationships of metazoan phyla on the basis of mitochondrial genome arrangements while incorporating prior knowledge of the monophyly of various groups from other sources. The work we present here differs from our previous work in the statistics literature in that (1) we incorporate prior information on classifications of metazoans at the phylum level, (2) we describe several advances in our computational approach, and (3) we analyze a much larger data set (87 taxa) that consists of each unique, complete mitochondrial genome arrangement with a full complement of 37 genes that were present in the NCBI (National Center for Biotechnology Information) database at a recent date. In addition, we analyze a subset of 28 of these 87 taxa for which the non-tRNA mitochondrial genomes are unique where the assumption of our inversion-only model of rearrangement is more plausible. We present summaries of Bayesian posterior distributions of tree topology on the basis of these two data sets.     

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.     

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.     

Phylogenetic information from three mitochondrial genomes of Terebelliformia (Annelida) worms and duplication of the methionine tRNA

Mitochondrial genomes have been useful for inferring animal phylogeny across a wide range of clades, however they are still poorly sampled in some animal taxa, limiting our knowledge of mtDNA evolution. For example, despite being one of the most diverse animal phyla, only 5 complete annelid mitochrondial genomes have been published. To address this paucity of information, we obtained complete mitochondrial genomic sequences from Pista cristata (Terebellidae) and Terebellides stroemi (Trichobranchidae) as well as one nearly complete mitochondrial genome from Eclysippe vanelli (Ampharetidae). These taxa are within Terebelliformia (Annelida), which include spaghetti worms, icecream cone worms and their relatives. In contrast to the 37 genes found in most bilaterian metazoans, we recover 38 genes in the mitochondrial genomes of T. stroemi and P. cristata due to the presence of a second methionine tRNA (trnM). Interestingly, the two trnMs are located next to each other and are possibly a synapomorphy of these two taxa. The E. vanelli partial mitochondrial genome lacks this additional trnM at the same position, but it may be present in the region not sampled. Compared to other annelids, gene orders of these three mitochondrial genomes are generally conserved except for the atp6-mSSU region. Phylogenetic analyses reveal that mtDNA data strongly supports a Trichobranchidae/Terebellidae clade.     

Testing the new animal phylogeny: a phylum level molecular analysis of the animal kingdom

The new animal phylogeny inferred from ribosomal genes some years ago has prompted a number of radical rearrangements of the traditional, morphology based metazoan tree. The two main bilaterian clades, Deuterostomia and Protostomia, find strong support, but the protostomes consist of two sister groups, Ecdysozoa and Lophotrochozoa, not seen in morphology based trees. Although widely accepted, not all recent molecular phylogenetic analyses have supported the tripartite structure of the new animal phylogeny. Furthermore, even if the small ribosomal subunit (SSU) based phylogeny is correct, there is a frustrating lack of resolution of relationships between the phyla that make up the three clades of this tree. To address this issue, we have assembled a dataset including a large number of aligned sequence positions as well as a broad sampling of metazoan phyla. Our dataset consists of sequence data from ribosomal and mitochondrial genes combined with new data from protein coding genes (5139 amino acid and 3524 nucleotide positions in total) from 37 representative taxa sampled across the Metazoa. Our data show strong support for the basic structure of the new animal phylogeny as well as for the Mandibulata including Myriapoda. We also provide some resolution within the Lophotrochozoa, where we confirm support for a monophyletic clade of Echiura, Sipuncula and Annelida and surprising evidence of a close relationship between Brachiopoda and Nemertea.     

Early evolution of the bilateria

The phylogeny of the Bilateria and especially the early steps in the evolution of the bilaterian bauplan are still a controversial topic. In this context the relationships of the platyhelminths and the nematodes play a crucial role. Previous molecular studies of the relationships of these groups, which were based on 18S ribosomal DNA sequences, yielded conflicting results. In the present study a new framework is developed for the phylogenetic analysis of bilaterian relationships, using concatenated amino acid sequences of several nuclear genes. In this analysis, the rhabditophoran platyhelminths are probably the sister group of all other analyzed Bilateria, the Eubilateria, which are characterized by a one-way intestine with an anus. The Eubilateria are split into the nematode lineage and the coelomates. The phylogenetic results of the present study indicate that genetic features found in the model organisms Caenorhabditis and Drosophila might be found in all Eubilateria. Estimations of the divergence times show that the major bilaterian phyla did not originate in an explosive radiation during the Cambrian but rather that the Bilateria have a several hundred million years long Precambrian history.     

Assessing the root of bilaterian animals with scalable phylogenomic methods

A clear picture of animal relationships is a prerequisite to understand how the morphological and ecological diversity of animals evolved over time. Among others, the placement of the acoelomorph flatworms, Acoela and Nemertodermatida, has fundamental implications for the origin and evolution of various animal organ systems. Their position, however, has been inconsistent in phylogenetic studies using one or several genes. Furthermore, Acoela has been among the least stable taxa in recent animal phylogenomic analyses, which simultaneously examine many genes from many species, while Nemertodermatida has not been sampled in any phylogenomic study. New sequence data are presented here from organisms targeted for their instability or lack of representation in prior analyses, and are analysed in combination with other publicly available data. We also designed new automated explicit methods for identifying and selecting common genes across different species, and developed highly optimized supercomputing tools to reconstruct relationships from gene sequences. The results of the work corroborate several recently established findings about animal relationships and provide new support for the placement of other groups. These new data and methods strongly uphold previous suggestions that Acoelomorpha is sister clade to all other bilaterian animals, find diminishing evidence for the placement of the enigmatic Xenoturbella within Deuterostomia, and place Cycliophora with Entoprocta and Ectoprocta. The work highlights the implications that these arrangements have for metazoan evolution and permits a clearer picture of ancestral morphologies and life histories in the deep past.     

Phylogenetic analysis of the Wnt gene family. Insights from lophotrochozoan members

The Wnt gene family encodes secreted signaling molecules that control cell fate specification, proliferation, polarity, and movements during animal development. We investigate here the evolutionary history of this large multigenic family. Wnt genes have been almost exclusively isolated from two of the three main subdivisions of bilaterian animals, the deuterostomes (which include chordates and echinoderms) and the ecdysozoans (e.g., arthropods and nematodes). However, orthology relationships between deuterostome and ecdysozoan Wnt genes, and, more generally, the phylogeny of the Wnt family, are not yet clear. We report here the isolation of several Wnt genes from two species, the annelid Platynereis dumerilii and the mollusc Patella vulgata, which both belong to the third large bilaterian clade, the lophotrochozoans (which constitute, together with ecdysozoans, the protostomes). Multiple phylogenetic analyses of these sequences with a large set of other Wnt gene sequences, in particular, the complete set of Wnt genes of human, nematode, and fly, allow us to subdivide the Wnt family into 12 subfamilies. At least nine of them were already present in the last common ancestor of all bilaterian animals, and this further highlights the genetic complexity of this ancestor. The orthology relationships we present here open new perspectives for future developmental comparisons.     

Who came first--larvae or adults? origins of bilaterian metazoan larvae

There is a classic controversy in zoology over whether the common ancestor of living bilaterian phyla was a benthic animal with a bilaterian body plan, or was a pelagic larva-like animal similar to what we see today in the primary larvae of indirect-developing bilaterians. We examine the current larva-like adult hypothesis, and present an alternate model for the evolution of complex life histories by intercalation of larval features into the ontogeny of an ancestral direct-developing bilaterian. This gradual accumulation of larval features results in a developmental regulatory program that produces a larva distinct in body plan from the adult. The evolution of a rapid and complete metamorphosis is made possible by the convergent evolution of set aside cells in the final stages of the emergence of indirect developing larval forms. Although convergences abound either hypothesis for the evolution of developmental pathways and life histories, the bilaterian first hypothesis is consistent with all stages of evolution of a complex life history being selectively advantageous, with the rapid evolution of larval forms, and with the frequent co-option of genes from the adult phase of the life cycle prevalent in the evolution of embryos and larvae.     

Estimation of ancestral gene set of bilaterian animals and its implication to dynamic change of gene content in bilaterian evolution

To understand the process of bilaterian evolution, we estimated ancestral gene sets at the split of plant-animal-fungi and the divergence of bilaterian animals and from 1,236,790 non-redundant genes. We, then, examined how the numbers of the gene clusters have changed since the split. As a result, we estimated the numbers of gene clusters in the ancestral gene sets of plant-animal-fungi and bilaterian animals to be at least 2469 and 6577, respectively. Thus, we found a 2.7-fold increase in the number of gene clusters during the period from the evolutionary split of plant-animal-fungi to the divergence of bilaterian animals. Moreover, when we compared these numbers of ancestral gene clusters with those of extant animals such as the nematode, fly, mouse and human, we found that the extant bilaterian animals have retained more than 3500 gene clusters of the ancestral gene set, and have lost more than 1600 gene clusters. It suggests that these processes of genomic diversification provided bilaterian animals with molecular basis for species diversity.     

The Radiata and the evolutionary origins of the bilaterian body plan

The apparent conservation of cellular and molecular developmental mechanisms observed in a handful of bilaterian metazoans has spawned a "race" to reconstruct the bilaterian ancestor. Knowledge of this ancestor would permit us to reconstruct the evolutionary changes that have occurred along specific bilaterian lineages. However, comparisons among extant bilaterians provide an unnecessarily limited view of the ancestral bilaterian. Since the original bilaterians are believed by many to be derived from a radially symmetrical ancestor, additional evidence might be obtained by examining present-day radially symmetrical animals. We briefly review pertinent features of the body plans of the extant radial eumetazoan phyla, the Cnidaria, and Ctenophora, in the context of revealing potential evolutionary links to the bilaterians.