Origins of the other metazoan body plans: the evolution of larval forms

Bilaterian animal body plan origins are not solely about adult forms. Most animals have larvae with body plans, ontogenies and ecologies distinct from adults. There are two primary hypotheses for larval origins. The first hypothesis suggests that the first animals were small pelagic forms similar to modern larvae, with adult bilaterian body plans evolved subsequently. The second hypothesis suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolation of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. If primitive metazoans were like modern larvae and distinct adult forms evolved independently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morphological convergence, but with distinct patterning genes, and this is observed. Thus, comparative studies of gene expression support independent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as being primitive, with planktonic larvae arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.     

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.     

Network evolution of body plans

One of the major goals in evolutionary developmental biology is to understand the relationship between gene regulatory networks and the diverse morphologies and their functionalities. Are the diversities solely triggered by random events, or are they inevitable outcomes of an interplay between evolving gene networks and natural selection? Segmentation in arthropod embryogenesis represents a well-known example of body plan diversity. Striped patterns of gene expression that lead to the future body segments appear simultaneously or sequentially in long and short germ-band development, respectively. Moreover, a combination of both is found in intermediate germ-band development. Regulatory genes relevant for stripe formation are evolutionarily conserved among arthropods, therefore the differences in the observed traits are thought to have originated from how the genes are wired. To reveal the basic differences in the network structure, we have numerically evolved hundreds of gene regulatory networks that produce striped patterns of gene expression. By analyzing the topologies of the generated networks, we show that the characteristics of stripe formation in long and short germ-band development are determined by Feed-Forward Loops (FFLs) and negative Feed-Back Loops (FBLs) respectively, and those of intermediate germ-band development are determined by the interconnections between FFL and negative FBL. Network architectures, gene expression patterns and knockout responses exhibited by the artificially evolved networks agree with those reported in the fly Drosophila melanogaster and the beetle Tribolium castaneum. For other arthropod species, principal network architectures that remain largely unknown are predicted. Our results suggest that the emergence of the three modes of body segmentation in arthropods is an inherent property of the evolving networks.     

Hierarchical evolution of animal body plans

An open question in animal evolution is why the phylum- and superphylum-level body plans have changed so little, while the class- and family-level body plans have changed so greatly since the early Cambrian. Davidson and Erwin (Davidson and Erwin, 2006; Erwin and Davidson, 2009) proposed that the hierarchical structure of gene regulatory networks leads to different observed evolutionary rates for terminal properties of the body plan versus major aspects of body plan morphology. Here, we calculated the speed of evolution of genes in these gene regulatory networks. We found that the genes which determine the phylum and superphylum characters evolve slowly, while those genes which determine the classes, families, and speciation evolve more rapidly. This result furnishes genetic support to the hypothesis that the hierarchical structure of developmental regulatory networks provides an organizing structure which guides the evolution of aspects of the body plan.     

Combinatorial model for the formation of body plans in higher metazoan taxa: Paleontological insight

The body plans of higher metazoan taxa were formed during a short time (on the geological time scale) by combination of the previously developed characters. The combinations were realized as a result of manifestation of latent characters in adults through various heterochronies. This resulted in mosaic evolution and concealment of intermediate forms. Many characters of new body plans appeared in the ancestral taxon and their various combinations in the newly established taxa formed the archaic diversity. The maximum rank of newly appearing higher taxa decreased with geological time. The evolution of metazoans passed from the development of the general body plan to less significant details and appearance of body plans describing taxa of lower ranks. New body plans of higher taxa were superposed on the old body plan rather than replaced it, extending with time the subordination of body plans and respective hierarchy of taxa. Aromorphoses are always connected with the appearance of a new body plan. The appearance of new taxa and an increase in morphological diversity mostly occurred at certain boundaries in the development of the biota, which were connected with a sharp increase in the previously limited resources.     

Cnidarian milestones in metazoan evolution

Cnidarians display most of the characters considered as milestonesof metazoan evolution. Whereas a tissue-level organization wasprobably already present in the multicellular common ancestorof all animals, the Urmetazoa, the emergence of important animalfeatures such as bilateral symmetry, triploblasty, a polarizednervous system, sense organs (eyes, statocysts), and a (chitinousor calcium-based) continuous skeleton can be traced back beforethe divergence between cnidarians and bilaterians. Modularityand metamery might be also regarded as two faces of the samemedal, likely involving conserved molecular mechanisms rulinganimal body architectures through regional specification ofiterated units. Available evidence indicates that the commonancestor of cnidarians and bilaterians, the UrEumetazoa, wasa surprisingly complex animal with nerve cell differentiation.We suggest that paedomorphic events in descendants of this ancestorled to the array of diversity seen in the main extant animalphyla. The use of molecular analyses and identifying the geneticdeterminants of anatomical organizations can provide an integrativetest of hypotheses of homologies and independent evidence ofthe evolutionary relationships among extant taxa.     

Evolution of animal body plans: the role of metazoan phylogeny at the interface between pattern and process

SUMMARY Comprehensive integrative studies are the hallmark of evolutionary developmental biology. A properly defined phylogenetic framework takes a central place in such analyses as the meeting ground for observation and inference. Molecular phylogenies take this place in many current studies on animal body plan evolution. In particular, 18S rRNA/DNA sequence analyses have yielded a new view of animal evolution that is often contrasted with a presumed traditional or classical view. First, I expose this traditional view to be a simplified historical abstraction that became textbook dogma. Second, I discuss how two recent important studies of animal body plan evolution, examining the evolution of the platyhelminth body plan and the evolutionary significance of indirect development and set-aside cells, have actively incorporated two problematic aspects of the newly emerging molecular view of animal evolution: incomplete and unresolved phylogenies.     

Gene duplications in early metazoan evolution

Major increases in complexity during animal evolution occurred at the transition from a unicellular protozoan to a multicellular metazoan, the evolution of Bilateria from diploblasts (possibly the Cambrian explosion) and during early vertebrate evolution. A role for gene duplication in the third event has been widely discussed. Here I examine the possible role of gene duplications and domain shuffling in the first two events. There is evidence for a wave of gene duplications and shuffling which may have paved the way for multicellularity; there are also examples of gene duplications that may have facilitated the transition from diploblasts to Bilateria.     

The evolution of metazoan extracellular matrix

The modular domain structure of extracellular matrix (ECM) proteins and their genes has allowed extensive exon/domain shuffling during evolution to generate hundreds of ECM proteins. Many of these arose early during metazoan evolution and have been highly conserved ever since. Others have undergone duplication and divergence during evolution, and novel combinations of domains have evolved to generate new ECM proteins, particularly in the vertebrate lineage. The recent sequencing of several genomes has revealed many details of this conservation and evolution of ECM proteins to serve diverse functions in metazoa.     

Conservation and diversification of Msx protein in metazoan evolution

Msx (/msh) family genes encode homeodomain (HD) proteins that control ontogeny in many animal species. We compared the structures of Msx genes from a wide range of Metazoa (Porifera, Cnidaria, Nematoda, Arthropoda, Tardigrada, Platyhelminthes, Mollusca, Brachiopoda, Annelida, Echiura, Echinodermata, Hemichordata, and Chordata) to gain an understanding of the role of these genes in phylogeny. Exon-intron boundary analysis suggested that the position of the intron located N-terminally to the HDs was widely conserved in all the genes examined, including those of cnidarians. Amino acid (aa) sequence comparison revealed 3 new evolutionarily conserved domains, as well as very strong conservation of the HDs. Two of the three domains were associated with Groucho-like protein binding in both a vertebrate and a cnidarian Msx homolog, suggesting that the interaction between Groucho-like proteins and Msx proteins was established in eumetazoan ancestors. Pairwise comparison among the collected HDs and their C-flanking aa sequences revealed that the degree of sequence conservation varied depending on the animal taxa from which the sequences were derived. Highly conserved Msx genes were identified in the Vertebrata, Cephalochordata, Hemichordata, Echinodermata, Mollusca, Brachiopoda, and Anthozoa. The wide distribution of the conserved sequences in the animal phylogenetic tree suggested that metazoan ancestors had already acquired a set of conserved domains of the current Msx family genes. Interestingly, although strongly conserved sequences were recovered from the Vertebrata, Cephalochordata, and Anthozoa, the sequences from the Urochordata and Hydrozoa showed weak conservation. Because the Vertebrata-Cephalochordata-Urochordata and Anthozoa-Hydrozoa represent sister groups in the Chordata and Cnidaria, respectively, Msx sequence diversification may have occurred differentially in the course of evolution. We speculate that selective loss of the conserved domains in Msx family proteins contributed to the diversification of animal body organization.     

The evolution of metazoan axial properties

Renewed interest in the developmental basis of organismal complexity, and the emergence of new molecular tools, is improving our ability to study the evolution of metazoan body plans. The most substantial changes in body-plan organization occurred early in metazoan evolution; new model systems for studying basal metazoans are now being developed, and total-genome-sequencing initiatives are underway for at least three of the four most important taxa. The elucidation of how the gene networks that are involved in axial organization, germ-layer formation and cell differentiation are used differently during development is generating a more detailed understanding of the events that have led to the current diversity of multicellular life.     

Early evolution of metazoan serine/threonine and tyrosine kinases: identification of selected kinases in marine sponges

The phylum Porifera (sponges) was the first to diverge from the common ancestor of the Metazoa. In this study, six cDNAs coding for protein- serine/threonine kinases (PS/TKs) are presented; they have been isolated from libraries obtained from the demosponges Geodia cydonium and Suberites domuncula and from the calcareous sponge Sycon raphanus. Sequence alignments of the catalytic domains revealed that two major families of PS/TK, the "conventional" (Ca(2+)-dependent) protein kinase C (PKC), the cPKC subfamily, as well as the "novel" (Ca(2+)- independent) PKC (nPKC), form two separate clusters. In each cluster, the sequence from S. raphanus diverges first. To approach the question about the origin of protein-tyrosine kinases (PTK), which are found only in Metazoa, we analyzed two additional PS/TKs which have been cloned from S. domuncula: the stress-responsive protein kinase (KRSvSD) and the protein-kinase-C-related kinase (PRKvSD). The construction of the phylogenetic tree, comprising the eight PS/TKs and the PTK cloned previously from G. cydonium, revealed that the PTK derived from the branch including the KRSvSD kinase. These data facilitate the first molecular approach to elucidate the origin of metazoan PTK within the PS/TK superfamily.      

Molecular evolution of the MAGUK family in metazoan genomes

Background  

Development, differentiation and physiology of metazoans all depend on cell to cell communication and subsequent intracellular signal transduction. Often, these processes are orchestrated via sites of specialized cell-cell contact and involve receptors, adhesion molecules and scaffolding proteins. Several of these scaffolding proteins important for synaptic and cellular junctions belong to the large family of membrane-associated guanylate kinases (MAGUK). In order to elucidate the origin and the evolutionary history of the MAGUKs we investigated full-length cDNA, EST and genomic sequences of species in major phyla.