Evolution of the Multicellular Animals

SYNOPSIS. Molecular sequence analysis is providing new insightsinto the study of metazoan relationships. The use of ribosomalRNA sequences is revising many of the metazoan phylogenies thathave been established traditionally with anatomical and embryologicaldata. Four new findings that seem to be well supported by moleculardata, both from the authors' laboratories and from others, aredescribed and discussed. First, the arthropods are members ofa deep primary clade within the protostomes and are not thesister taxa of either the annelids or the mollusks. Second,the lophophorate animals are clearly protostomes and are containedwithin a lophotrochozoan superclade including the mollusks,annelids, and many other phyla. Third, the arthropods togetherwith all other molting animals comprise a second monophyleticsuperclade within the protostomes, the ecdysozoa. Fourth, theplatyhelminthes are contained within the lophotrochozoan superclade.     

A Brief Review of Metazoan Phylogeny and Future Prospects in Hox-Research

Underlying any analysis on the evolution of development is aphylogenetic framework, whether explicitly stated or implied.As such, differing views on phylogenetic relationships leadto variable interpretations of how developmental mechanismshave changed through time. Over the past decade, many long-standinghypotheses about animal evolution have been questioned causingsubstantial changes in the assumed phylogenetic framework underlyingcomparative developmental studies. Current hypotheses aboutearly metazoan history suggest that three, not two, major lineagesof bilateral animals originated in the Precambrian: the Deuterostomes(e.g., seastars, acorn worms, and vertebrates), the Ecdysozoans(e.g., nematodes and arthropods), and the Lophotrochozoans (e.g.,annelids, mollusks, and lophophorates). Although informationin Hox-genes bears directly on our understanding of early metazoanevolution and the formation of body plans, research effort hasbeen focused primarily on two taxa, insects and vertebrates.By sampling a greater diversity of metazoan taxa and takingadvantage of biotechnological advances in genomics, we willnot only learn more about metazoan phylogeny, but will alsogain valuable insight as to the key evolutionary forces thatestablished and maintained metazoan bauplans.     

Three-dimensional reconstruction of mushroom body neuropils in the polychaete species <Emphasis Type="Italic">Nereis diversicolor</Emphasis> and <Emphasis Type="Italic">Harmothoe areolata</Emphasis> (Phyllodocida,Annelida)

Mushroom bodies are prominent brain neuropils present in most arthropod representatives. Similar structures in the brain of certain polychaete species are possibly homologous to these structures. Using three-dimensional reconstruction techniques, we investigated the structural composition of the mushroom body neuropils in the polychaete species Nereis diversicolor and Harmothoe areolata. Comparative analysis revealed a common organization of neuropil substructures in both species that closely matches the basic assembly of arthropod mushroom bodies. Concurring with earlier homology assessments, these neuroarchitectural similarities provide support for a common origin of mushroom body neuropils in polychaetes and arthropods. Beyond that, differences in the morphological differentiation of neuropil substructures indicate polychaete mushroom bodies to show a high degree of morphological variability, thus impeding the quest for a common ground pattern of these brain centers.     

The evolution of the Hox cluster: insights from outgroups

Two burgeoning research trends are helping to reconstruct the evolution of the Hox cluster with greater detail and clarity. First, Hox genes are being studied in a broader phylogenetic sampling of taxa: the past year has witnessed important new data from teleost fishes, onychophorans, myriapods, polychaetes, glossiphoniid leeches, ribbon worms, and sea anemones. Second, commonly accepted notions of animal relationships are being challenged by alternative phylogenetic hypotheses that are causing us to rethink the evolutionary relationships of important metazoan lineages, especially arthropods, annelids, nematodes, and platyhelminthes.     

Metazoan phylogeny and the Cambrian radiation

Sequence analysis of small-subunit ribosomal RNA (18S rRNA) has provided important new pieces for the great puzzle of metazoan phylogeny and has generated new perspectives on the Precambrian-Cambrian fossil record of the metazoan radiation. While the puzzle is far from resolved and the early results are plagued by difficulties in data analysis, intriguing insights have appeared. Early results suggest that molluscs and lophophorates are protostomes, and that deuterostomes may be derived from protostomes. More speculatively, annelids and molluscs may be derived from arthropods or an arthropod ancestor. The molecular evidence further strengthens paleontological arguments for an explosive metazoan radiation near the Vendian-Cambrian boundary, rather than a lengthy, but hidden, period of Precambrian diversification.     

The Position of Arthropods in the Animal Kingdom: A Search for a Reliable Outgroup for Internal Arthropod Phylogeny

Morphological evidence for the phylogeny of the animal kingdom has been discussed by numerous authors. DNA sequencing and phylogenetic methods for analyzing these data are alternative approaches to animal phylogeny, but the phenomenon of long branch attraction and poor taxonomic sampling have caused misinterpretations of metazoan relationships. Here we report a cladistic approach to metazoan evolution including 133 18S rDNA sequences of 31 animal phyla. Despite the difficulties associated with analyzing large data sets, our data suggest that the Bilateria and Protostomia are monophyletic. The internal phylogeny of the protostomes is divided into two main clades. One clade includes the classical protostome worms (annelids, sipunculans, echiurans, pogonophorans, and vestimentiferans), mollusks, nemerteans, “lophophorates,” platyhelminths, rotiferans, and acanthocephalans, although the internal resolution of the clade is very low. The second clade includes arthropods and other molting animals: tardigrades, onychophorans, nematodes, nematomorphans, kinorhynchs, and priapulans. The arthropods and related phyla lack a ciliated larvae, lack a multiciliate (locomotory) epithelium, and share many features, notably, a reduced coelomic cavity and the presence of a cuticle which molts. The use of these outgroups within the molting clade to root arthropod phylogenies is recommended instead of using annelids or other spiralians. The data are quite conclusive in those phyla with a good taxonomic sampling (i.e., platyhelminths and arthropods).     

Primary structures of the 5S ribosomal RNAs of 11 arthropods and applicability of 5S RNA to the study of metazoan evolution

Summary 5S Ribosomal RNA sequences have proven to be useful tools in the study of evolutionary relationships among species. However, in reviewing previously published trees constructed from alignments of metazoan 5S RNAs, we noticed several discrepancies with classical evolutionary views. One such discrepancy concerned the phylum Arthropoda, where a crustacean,Artemia salina, seemed to be evolutionarily very remote from four insects. The cause of this phenomenon was studied by determining the 5S RNA sequences of additional arthropods, viz.Limulus polyphemus, Eurypelma californica, Lasiodora erythrocythara, Areneus diadematus, Daphnia magna, Ligia oceanica, Homarus gammarus, Cancer pagurus, Spirobolus sp.,Locusta migratoria, andTenebrio molitor. A tree was then constructed from a dissimilarity matrix by a clustering method known as weighted pair grouping. Application of a correction for unequal evolutionary rates improved the apparent evolutionary position of the arthropods and of some other metazoan species. However, neither the uncorrected nor the corrected tree permitted a completely acceptable reconstruction of metazoan evolution. We presume that this phenomenon is due to random deviations in the evolutionary rate of 5S RNA.Presented at the FEBS Symposium on Genome Organization and Evolution, held in Crete, Greece, September 1–5, 1986     

The complete mitochondrial genome sequence of Whitmania pigra (Annelida, Hirudinea): the first representative from the class Hirudinea

The mitochondrial genome is a significant tool for investigating the evolutionary history of metazoan animals. The currently available mitochondrial genome data in GenBank is limited to understand the detail evolutionary relationship among the metazoan animals, especially in the phylum Annelida. Here we present the mitochondrial gene organization, gene order and codon usage of the leech Whitmania pigra (Annelida), which is the first representative from the class Hirudinea. It is a circular molecule of 14,426bp, and encodes 13 protein-coding genes, 2 ribosomal RNA genes, and 22 transfer RNA genes. All 37 genes of W. pigra mitochondrial genome are transcribed from the same strand, which is identical to studied annelids, two echiurans, two sipunculans and many other lophotrochozoans. Five conserved gene clusters can be found in mitochondrial genomes of nine studied annelids, including (1) cox1-N-cox2; (2) cox3-Q-nad6-cob-W-atp6; (3) H-nad5-F-E-P-T-nad4L-nad4; (4) srRNA-V-lrRNA; and (5) nad3-S(1)-nad2. Compared with that of other studied annelids, translocations of transfer RNAs were found in the gene arrangement of W. pigra mitochondrial genome. Phylogenetic analysis strongly support that the species from Hirudinina and Oligochaeta form a monophyletic group Clitellata (BPM=100, BPP=100), which is consistent with previous research based on morphological and other molecular data. Both gene order data and amino acid sequences reveal that echiurans are derived annelids and sipunculans should be clustered with annelids and echiurans.     

Introduction to ‘Homology and convergence in nervous system evolution’

The origin of brains and central nervous systems (CNSs) is thought to have occurred before the Palaeozoic era 540 Ma. Yet in the absence of tangible evidence, there has been continued debate whether today''s brains and nervous systems derive from one ancestral origin or whether similarities among them are due to convergent evolution. With the advent of molecular developmental genetics and genomics, it has become clear that homology is a concept that applies not only to morphologies, but also to genes, developmental processes, as well as to behaviours. Comparative studies in phyla ranging from annelids and arthropods to mammals are providing evidence that corresponding developmental genetic mechanisms act not only in dorso–ventral and anterior–posterior axis specification but also in segmentation, neurogenesis, axogenesis and eye/photoreceptor cell formation that appear to be conserved throughout the animal kingdom. These data are supported by recent studies which identified Mid-Cambrian fossils with preserved soft body parts that present segmental arrangements in brains typical of modern arthropods, and similarly organized brain centres and circuits across phyla that may reflect genealogical correspondence and control similar behavioural manifestations. Moreover, congruence between genetic and geological fossil records support the notion that by the ‘Cambrian explosion’ arthropods and chordates shared similarities in brain and nervous system organization. However, these similarities are strikingly absent in several sister- and outgroups of arthropods and chordates which raises several questions, foremost among them: what kind of natural laws and mechanisms underlie the convergent evolution of such similarities? And, vice versa: what are the selection pressures and genetic mechanisms underlying the possible loss or reduction of brains and CNSs in multiple lineages during the course of evolution? These questions were addressed at a Royal Society meeting to discuss homology and convergence in nervous system evolution. By integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, the meeting covered disparities in nervous system origins as well as correspondences of neural circuit organization and behaviours, all of which allow evidence-based debates for and against the proposition that the nervous systems and brains of animals might derive from a common ancestor.     

Phosphatized rare star-like mouth disc of Punctatus and its functional morphology from the earliest Cambrian of the South Shaanxi China

The Meishucun stage is the prelude in deciphering the Cambrian Explosion. In this prominent stage, rapid radioactive evolution and body-plan innovation have taken place and different associations of organism have been shaped. In this paper we report several 3D-preserved rare star-like fossils with finely preserved soft tissues which were recovered from the Kuanchuanpu Member of the Dengying Formation in South Shaanxi, China in 2003. By studying on functional morphology and analogy with mouthpart of Punctatus, there are evidences that this star-like organism approaches the coelenterates in systematic classification and the centre of star-like organism is its mouth. The appearance of coelenterates marks the real beginning of metazoan evolution. Therefore, it has the prominent position in the origin and evolutionary history of organisms. Perhaps the star-like organism represents the early types of coelenterate with original tentacles. These new materials provide new evidence for the origin, evolution and the functional evolution of the metazoan during the early stage of the Cambrian Explosion. __________ Translated from Acta Micropalaeontologica Sinica, 2006, 23(1): 62–69 [译自: 微体古生物学报]     

Comparison of microglomerular structures in the mushroom body calyx of neopteran insects

Mushroom bodies (MBs) are prominent neuropils in the insect brain involved in higher order processing such as sensory integration, learning and memory, and spatial orientation. The size and general morphology of MBs are diverse across insects. In this study we comparatively investigated the microstructure of synaptic complexes (microglomeruli) in major sensory input regions of the MBs, the calyces, across various neopteran insect species. Pre- and postsynaptic compartments of microglomeruli were analyzed using anti-synapsin immunocytochemistry, f-actin-phalloidin labeling and high-resolution confocal microscopy. Our results suggest that calycal microglomeruli are present across all investigated neopteran insect species, but differences are found in the distribution of synapsin and f-actin within their pre- and postsynaptic compartments. Hymenopteran MBs contain the highest number and packing density of microglomeruli compared to all other species from the different insect orders we investigated. We conclude that the evolution of high numbers of microglomeruli in Hymenoptera may reflect an increase in synaptic microcircuits, which could enhance the computational capacities of the MBs.     

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.     

Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation

The origin of animal segmentation, the periodic repetition of anatomical structures along the anteroposterior axis, is a long-standing issue that has been recently revived by comparative developmental genetics. In particular, a similar extensive morphological segmentation (or metamerism) is commonly recognized in annelids and arthropods. Mostly based on this supposedly homologous segmentation, these phyla have been united for a long time into the clade Articulata. However, recent phylogenetic analysis dismissed the Articulata and thus challenged the segmentation homology hypothesis. Here, we report the expression patterns of genes orthologous to the arthropod segmentation genes engrailed and wingless in the annelid Platynereis dumerilii. In Platynereis, engrailed and wingless are expressed in continuous ectodermal stripes on either side of the segmental boundary before, during, and after its formation; this expression pattern suggests that these genes are involved in segment formation. The striking similarities of engrailed and wingless expressions in Platynereis and arthropods may be due to evolutionary convergence or common heritage. In agreement with similarities in segment ontogeny and morphological organization in arthropods and annelids, we interpret our results as molecular evidence of a segmented ancestor of protostomes.     

陕南早寒武世具口部的磷酸盐化Punctatus及其胚胎化石

报道陕西南部灯影组宽川铺段地层中发现的Punctatus锥体标本、保留精美软组织特征的口部标本和可能的胚胎标本。对Punctatus软组织及整体形态功能研究表明,Punctatus在分类上可能更接近于腔肠动物的水螅型,代表初具原始触手的腔肠动物早期演化类型。在上万枚与Punctatus共生的球状化石中,发现若干枚可能的原肠期胚胎及胚胎发育晚期标本,在此基础上提出PunctatusemeiensisHe,1980花冠状口部可能经历的胚胎发育序列。     

Phylogenetic relationships of annelids,molluscs, and arthropods evidenced from molecules and morphology

Annelids and arthropods have long been considered each other's closest relatives, as evidenced by similarities in their segmented body plans. An alternative view, more recently advocated by investigators who have examined partial 18S ribosomal RNA data, proposes that annelids, molluscs, and certain other minor phyla with trochophore larva stages share a more recent common ancestor with one another than any do with arthropods. The two hypotheses are mutually exclusive in explaining spiralian relationships. Cladistic analysis of morphological data does not reveal phylogentic relationships among major spiralian taxa but does suggest monophyly for both the annelids and molluscs. Distance and maximum-likelihood analyses of 18S rRNA gene sequences from major spiralian taxa suggest a sister relationship between annelids and molluscs and provide a clear resolution within the major groups of the spiralians. The parsimonious tree based on molecular data, however, indicates a sister relationship of the Annelida and Bivalvia, and an earlier divergence of the Gastropoda than the Annelida–Bivalvia clade. To test further hypotheses on the phylogenetic relationships among annelids, molluscs, and arthropods, and the ingroup relationships within the major spiralian taxa, we combine the molecular and morphological data sets and subject the combined data matrix to parsimony analysis. The resulting tree suggests that the molluscs and annelids form a monophyletic lineage and unites the molluscan taxa to a monophyletic group. Therefore, the result supports the Eutrochozoa hypothesis and the monophyly of molluscs, and indicates early acquisition of segmented body plans in arthropods. Received: 25 September 1995 / Accepted: 15 March 1996     

陕南早寒武世早期Quadrapyrgites再研究

处于"寒武纪生命大爆发"序幕阶段的梅树村期,生物类群大规模辐射,身体构型快速革新,与前寒武纪生物群面貌明显不同.最近在陕南宁强宽川铺地区梅树村期地层中发现了大量五辐射Punctatus及部分四辐射四方塔形壳属Quadrapyrgites,其中包括1个新种Quadrnpyrgites undulatuscostalis sp.nov..在此基础上对Quadrapyrgites进行了属征补充.双胚层腔肠动物的出现标志着地球生命史的真后生动物演化开端,在生物起源演化历程上占据着关键的位置.本文为研究真后生动物起源演化、生物辐射、体型构建提供了重要实证.     

Comparative neuroanatomy suggests repeated reduction of neuroarchitectural complexity in Annelida

Background

Paired mushroom bodies, an unpaired central complex, and bilaterally arranged clusters of olfactory glomeruli are among the most distinctive components of arthropod neuroarchitecture. Mushroom body neuropils, unpaired midline neuropils, and olfactory glomeruli also occur in the brains of some polychaete annelids, showing varying degrees of morphological similarity to their arthropod counterparts. Attempts to elucidate the evolutionary origin of these neuropils and to deduce an ancestral ground pattern of annelid cerebral complexity are impeded by the incomplete knowledge of annelid phylogeny and by a lack of comparative neuroanatomical data for this group. The present account aims to provide new morphological data for a broad range of annelid taxa in order to trace the occurrence and variability of higher brain centers in segmented worms.

Results

Immunohistochemically stained preparations provide comparative neuroanatomical data for representatives from 22 annelid species. The most prominent neuropil structures to be encountered in the annelid brain are the paired mushroom bodies that occur in a number of polychaete taxa. Mushroom bodies can in some cases be demonstrated to be closely associated with clusters of spheroid neuropils reminiscent of arthropod olfactory glomeruli. Less distinctive subcompartments of the annelid brain are unpaired midline neuropils that bear a remote resemblance to similar components in the arthropod brain. The occurrence of higher brain centers such as mushroom bodies, olfactory glomeruli, and unpaired midline neuropils seems to be restricted to errant polychaetes.

Conclusions

The implications of an assumed homology between annelid and arthropod mushroom bodies are discussed in light of the 'new animal phylogeny'. It is concluded that the apparent homology of mushroom bodies in distantly related groups has to be interpreted as a plesiomorphy, pointing towards a considerably complex neuroarchitecture inherited from the last common ancestor, Urbilateria. Within the annelid radiation, the lack of mushroom bodies in certain groups is explained by widespread secondary reductions owing to selective pressures unfavorable for the differentiation of elaborate brains. Evolutionary pathways of mushroom body neuropils in errant polychaetes remain enigmatic.     

Prepro-tachykinin gene expression in the brain of the honeybee<Emphasis Type="Italic"> Apis mellifera</Emphasis>

We have recently identified a tachykinin-related peptide (AmTRP) from the mushroom bodies (MBs) of the brain of the honeybee Apis mellifera L. by using direct matrix-assisted laser desorption/ionization with time-of-flight mass spectometry and have isolated its cDNA. Here, we have examined prepro-AmTRP gene expression in the honeybee brain by using in situ hybridization. The prepro-AmTRP gene is expressed predominantly in the MBs and in some neurons located in the optic and antennal lobes. cDNA microarray studies have revealed that AmTRP expression is enriched in the MBs compared with other brain regions. There is no difference in AmTRP-expressing cells among worker, queen, and drone brains, suggesting that the cell types that express the prepro-AmTRP gene do not change according to division of labor, sex, or caste. The unique expression pattern of the prepro-AmTRP gene suggests that AmTRPs function as neuromodulators in the MBs of the honeybee brain.This work was supported by a Grant-in-Aid from the Bio-oriented Technology Research Advancement Institution (BRAIN)     

Phosphatized rare star-like mouth disc of Punctatus and its functional morphology from the earliest Cambrian of the South Shaanxi China

The Meishucun stage is the prelude in decipher-ing the Cambrian Explosion. In this prominent stage, rapid radioactive evolution and body-plan innovation have taken place and different associations of organism have been shaped. In this paper we report several 3D-preserved rare star-like fossils with finely preserved soft tissues which were recovered from the Kuanchuanpu Member of the Dengying Formation in South Shaanxi, China in 2003. By studying on functional morphology and analogy with mouthpart of Punctatus, there are evidences that this star-like organism approaches the coelenterates in systematic classification and the centre of star-like organism is its mouth. The appearance of coelenterates marks the real beginning of metazoan evolution. Therefore, it has the prominent position in the origin and evolutionary history of organisms. Perhaps the star-like organism represents the early types of coelenterate with original tentacles. These new materials provide new evidence for the origin, evolution and the functional evolution of the metazoan during the early stage of the Cambrian Explosion.     

Evolutionary aspects of octopaminergic systems with emphasis on arthropods

We review current knowledge on octopaminergic systems in all major phyla with emphasis on arthropods. Octopaminergic systems occur in all triploblastic animals investigated. Close relationships of the octopamine-receptors in protostomes to vertebrate alpha-adrenergic receptors suggest an ancient common origin. Some evidence suggests that the octopaminergic system may be younger than the vertebrate adrenergic system. All octopaminergic systems are constructed from comparatively few neurons, and the cell populations in different representatives of a given phylum are clearly similar. Current data do not allow any conclusions on the relationships between molluscs and annelids (Lophotrochozoa) to nematodes and arthropods (Ecdysozoa).In chelicerates, including Limulus as a remaining xiphosuran, and crustaceans, octopaminergic neurons occur in pairs. All investigated winged insects (Pterygota) possess similar arrangements of octopaminergic cell populations, suggesting that their octopaminergic systems have been largely conserved during evolution. Unpaired octopaminergic neurons, with symmetrical, bilaterally projecting efferent axons in insects do not appear to have counterparts in other arthropods. Unpaired-octopaminergic neurons may thus be an autapomorphic feature of winged insects. Octopamine acts as an inhibitory neurotransmitter in gastropods, and as an excitatory transmitter controlling bioluminescence in fireflies. Octopamine is also implicated in controlling bioluminescence in other phyla. All critically examined triploblastic invertebrates release octopamine as a hormone, as a peripheral modulator and as a central neuromodulator in the nervous system, which exerts its action via evolutionary related G-protein-coupled receptors that activate cAMP. The evolution of the octopaminergic system seems fundamental for the evolution of efficient locomotory mechanisms, complex social interactions, and cognitive abilities of arthropods.