Animal Body Plans Research Articles

Micromanagement of Drosophila Post-Embryonic Development by Hox Genes.

Hox genes function early in development to determine regional identity in animals. Consequently, the loss or gain of Hox gene expression can change this identity and cause homeotic transformations. Over 20 years ago, it was observed that the role of Hox genes in patterning animal body plans involves the fine-scale regulation of cell fate and identity during development, playing the role of ‘micromanagers’ as proposed by Michael Akam in key perspective papers. Therefore, as well as specifying where structures develop on animal bodies, Hox genes can help to precisely sculpt their morphology. Here, we review work that has provided important insights about the roles of Hox genes in influencing cell fate during post-embryonic development in Drosophila to regulate fine-scale patterning and morphology. We also explore how this is achieved through the regulation of Hox genes, specific co-factors and their complex regulation of hundreds of target genes. We argue that further investigating the regulation and roles of Hox genes in Drosophila post-embryonic development has great potential for understanding gene regulation, cell fate and phenotypic differentiation more generally.

Tardigrades and their emergence as model organisms.

Experimentally tractable organisms like C. elegans, Drosophila, zebrafish, and mouse are popular models for addressing diverse questions in biology. In 1997, two of the most valuable invertebrate model organisms to date-C. elegans and Drosophila-were found to be much more closely related to each other than expected. C. elegans and Drosophila belong to the nematodes and arthropods, respectively, and these two phyla and six other phyla make up a clade of molting animals referred to as the Ecdysozoa. The other ecdysozoan phyla could be valuable models for comparative biology, taking advantage of the rich and continual sources of research findings as well as tools from both C. elegans and Drosophila. But when the Ecdysozoa was first recognized, few tools were available for laboratory studies in any of these six other ecdysozoan phyla. In 1999 I began an effort to develop tools for studying one such phylum, the tardigrades. Here, I describe how the tardigrade species Hypsibius exemplaris and tardigrades more generally have emerged over the past two decades as valuable new models for answering diverse questions. To date, these questions have included how animal body plans evolve and how biological materials can survive some remarkably extreme conditions.

Dawn of complex animal food webs: A new predatory anthozoan (Cnidaria) from Cambrian

Cnidarians diverged very early in animal evolution; therefore, investigations of the morphology and trophic levels of early fossil cnidarians may provide critical insights into the evolution of metazoans and the origin of modern marine food webs. However, there has been a lack of unambiguous anthozoan cnidarians from Ediacaran assemblages, and undoubted anthozoans from the Cambrian radiation of metazoans are very rare and lacking in ecological evidence. Here, we report a new polypoid cnidarian, Nailiana elegans gen. et sp. nov., represented by multiple solitary specimens from the early Cambrian Chengjiang biota (∼520 Ma) of South China. These specimens show eight unbranched tentacles surrounding a single opening into the gastric cavity, which may have born multiple mesenteries. Thus, N. elegans displays a level of organization similar to that of extant cnidarians. Phylogenetic analyses place N. elegans in the stem lineage of Anthozoa and suggest that the ancestral anthozoan was a soft-bodied, solitary polyp showing octoradial symmetry. Moreover, one specimen of the new polyp preserves evidence of predation on an epifaunal lingulid brachiopod. This case provides the oldest direct evidence of macrophagous predation, the advent of which may have triggered the emergence of complex trophic/ecological relationships in Cambrian marine communities and spurred the explosive radiation of animal body plans.

Patterning with clocks and genetic cascades: Segmentation and regionalization of vertebrate versus insect body plans.

Oscillatory and sequential processes have been implicated in the spatial patterning of many embryonic tissues. For example, molecular clocks delimit segmental boundaries in vertebrates and insects and mediate lateral root formation in plants, whereas sequential gene activities are involved in the specification of regional identities of insect neuroblasts, vertebrate neural tube, vertebrate limb, and insect and vertebrate body axes. These processes take place in various tissues and organisms, and, hence, raise the question of what common themes and strategies they share. In this article, we review 2 processes that rely on the spatial regulation of periodic and sequential gene activities: segmentation and regionalization of the anterior–posterior (AP) axis of animal body plans. We study these processes in species that belong to 2 different phyla: vertebrates and insects. By contrasting 2 different processes (segmentation and regionalization) in species that belong to 2 distantly related phyla (arthropods and vertebrates), we elucidate the deep logic of patterning by oscillatory and sequential gene activities. Furthermore, in some of these organisms (e.g., the fruit fly Drosophila), a mode of AP patterning has evolved that seems not to overtly rely on oscillations or sequential gene activities, providing an opportunity to study the evolution of pattern formation mechanisms.

Local tissue interactions govern pLL patterning in medaka

Vertebrate organs are arranged in a stereotypic, species-specific position along the animal body plan. Substantial morphological variation exists between related species, especially so in the vastly diversified teleost clade. It is still unclear how tissues, organs and systems can accommodate such diverse scaffolds. Here, we use the distinctive arrangement of neuromasts in the posterior lateral line (pLL) system of medaka fish to address the tissue-interactions defining a pattern. We show that patterning in this peripheral nervous system is established by autonomous organ precursors independent of neuronal wiring. In addition, we target the keratin 15 gene to generate stuck-in-the-midline (siml) mutants, which display epithelial lesions and a disrupted pLL patterning. By using siml/wt chimeras, we determine that the aberrant siml pLL pattern depends on the mutant epithelium, since a wild type epithelium can rescue the siml phenotype. Inducing epithelial lesions by 2-photon laser ablation during pLL morphogenesis phenocopies siml genetic mutants and reveals that epithelial integrity defines the final position of the embryonic pLL neuromasts. Our results using the medaka pLL disentangle intrinsic from extrinsic properties during the establishment of a sensory system. We speculate that intrinsic programs guarantee proper organ morphogenesis, while instructive interactions from surrounding tissues facilitates the accommodation of sensory organs to the diverse body plans found among teleosts.

Studying evolution of the primary body axis in vivo and in vitro.

The metazoan body plan is established during early embryogenesis via collective cell rearrangements and evolutionarily conserved gene networks, as part of a process commonly referred to as gastrulation. While substantial progress has been achieved in terms of characterizing the embryonic development of several model organisms, underlying principles of many early patterning processes nevertheless remain enigmatic. Despite the diversity of (pre-)gastrulating embryo and adult body shapes across the animal kingdom, the body axes, which are arguably the most fundamental features, generally remain identical between phyla. Recently there has been a renewed appreciation of ex vivo and in vitro embryo-like systems to model early embryonic patterning events. Here, we briefly review key examples and propose that similarities in morphogenesis and associated gene expression dynamics may reveal an evolutionarily conserved developmental mode as well as provide further insights into the role of external or extraembryonic cues in shaping the early embryo. In summary, we argue that embryo-like systems can be employed to inform previously uncharted aspects of animal body plan evolution as well as associated patterning rules.

The developmental biology of Charnia and the eumetazoan affinity of the Ediacaran rangeomorphs.

Molecular timescales estimate that early animal lineages diverged tens of millions of years before their earliest unequivocal fossil evidence. The Ediacaran macrobiota (~574 to 538 million years ago) are largely eschewed from this debate, primarily due to their extreme phylogenetic uncertainty, but remain germane. We characterize the development of Charnia masoni and establish the affinity of rangeomorphs, among the oldest and most enigmatic components of the Ediacaran macrobiota. We provide the first direct evidence for the internal interconnected nature of rangeomorphs and show that Charnia was constructed of repeated branches that derived successively from pre-existing branches. We find homology and rationalize morphogenesis between disparate rangeomorph taxa, before producing a phylogenetic analysis, resolving Charnia as a stem-eumetazoan and expanding the anatomical disparity of that group to include a long-extinct bodyplan. These data bring competing records of early animal evolution into closer agreement, reformulating our understanding of the evolutionary emergence of animal bodyplans.

Septins and a formin have distinct functions in anaphase chiral cortical rotation in the Caenorhabditis elegans zygote.

Many cells and tissues exhibit chirality that stems from the chirality of proteins and polymers. In the Caenorhabditis elegans zygote, actomyosin contractility drives chiral rotation of the entire cortex circumferentially around the division plane during anaphase. How contractility is translated to cell-scale chirality, and what dictates handedness, are unknown. Septins are candidate contributors to cell-scale chirality because they anchor and cross-link the actomyosin cytoskeleton. We report that septins are required for anaphase cortical rotation. In contrast, the formin CYK-1, which we found to be enriched in the posterior in early anaphase, is not required for cortical rotation but contributes to its chirality. Simultaneous loss of septin and CYK-1 function led to abnormal and often reversed cortical rotation. Our results suggest that anaphase contractility leads to chiral rotation by releasing torsional stress generated during formin-based polymerization, which is polarized along the cell anterior–posterior axis and which accumulates due to actomyosin network connectivity. Our findings shed light on the molecular and physical bases for cellular chirality in the C. elegans zygote. We also identify conditions in which chiral rotation fails but animals are developmentally viable, opening avenues for future work on the relationship between early embryonic cellular chirality and animal body plan.

Exceptionally preserved early Cambrian bilaterian developmental stages from Mongolia

Fossilized invertebrate embryonic and later developmental stages are rare and restricted largely to the Ediacaran-Cambrian, providing direct insight into development during the emergence of animal bodyplans. Here we report a new assemblage of eggs, embryos and bilaterian post-embryonic developmental stages from the early Cambrian Salanygol Formation of Dzhabkan Microcontinent of Mongolia. The post-embryonic developmental stages of the bilaterian are preserved with cellular fidelity, possessing a series of bilaterally arranged ridges that compare to co-occurring camenellan sclerites in which the initial growth stages retain the cellular morphology of modified juveniles. In this work we identify these fossils as early post-embryonic developmental stages of camenellans, an early clade of stem-brachiopods, known previously only from isolated sclerites. This interpretation corroborates previous reconstructions of camenellan scleritomes with sclerites arranged in medial and peripheral concentric zones. It further supports the conjecture that molluscs and brachiopods are descended from an ancestral vermiform and slug-like bodyplan.

Molecular insights into deuterostome evolution from hemichordate developmental biology.

Hemichordates, along with echinoderms and chordates, belong to the lineage of bilaterians called the deuterostomes. Their phylogenetic position as an outgroup to chordates provides an opportunity to investigate the evolutionary origins of the chordate body plan and reconstruct ancestral deuterostome characters. The body plans of the hemichordates and chordates are organizationally divergent making anatomical comparisons very challenging. The developmental underpinnings of animal body plans are often more conservative than the body plans they regulate, and offer a novel data set for making comparisons between morphologically divergent body architectures. Here I review the hemichordate developmental data generated over the past 20 years that further test hypotheses of proposed morphological affinities between the two taxa, but also compare the conserved anteroposterior, dorsoventral axial patterning programs and germ layer specification programs. These data provide an opportunity to determine which developmental programs are ancestral deuterostome or bilaterian innovations, and which ones occurred in stem chordates or vertebrates representing developmental novelties of the chordate body plan.

Structural Basis of WLS/Evi-Mediated Wnt Transport and Secretion

Wnts are evolutionarily conserved ligands that signal at short range to regulate morphogenesis, cell fate, and stem cell renewal. The first and essential steps in Wnt secretion are their O-palmitoleation and subsequent loading onto the dedicated transporter Wntless/evenness interrupted (WLS/Evi). We report the 3.2Å resolution cryogenic electron microscopy (cryo-EM) structure of palmitoleated human WNT8A in complex with WLS. This is accompanied by biochemical experiments to probe the physiological implications of the observed association. The WLS membrane domain has close structural homology to G protein-coupled receptors (GPCRs). A Wnt hairpin inserts into a conserved hydrophobic cavity in the GPCR-like domain, and the palmitoleate protrudes between two helices into the bilayer. A conformational switch of highly conserved residues on a separate Wnt hairpin might contribute to its transfer to receiving cells. This work provides molecular-level insights into a central mechanism in animal body plan development and stem cell biology.

Behavioural imprint of the Ordovician Radiation: Evidence from Middle–Upper Ordovician deep-sea trace fossils in western Inner Mongolia, North China

Trace fossils are unique evidence of the body plan and behavioural complexity of animals. Major radiation periods in the Phanerozoic were associated with not only changes in biodiversity, biomass, and ecosystems but also transformations in the relatively implicit, behavioural world. Here we report on a diverse ichnoassemblage from the Middle–Upper Ordovician deep-marine deposits of Inner Mongolia, North China, totalling 24 ichnogenera (including two undetermined forms). They include Alcyonidiopsis, Bifasciculus, Bifungites, Chondrites, Circulichnis, ?Cochlichnus, Dendrorhaphe, Diplocraterion, Halopoa, Gyrophyllites, Monofungites, Multina, Nereites, Paleodictyon, Phymatoderma, Ptychoplasma, Rhizocorallium, Sinusichnus, Taenidium, Thalassinoides, Trichichnus, Zoophycos, bag-like trace, and closed ring trace. Highly regular and complex burrow systems have been discovered, i.e., the branched circular pattern of Circulichnis sinensis, elaborate radial graphoglyptid tunnel system Dendrorhaphe racemosa ichnosp. nov., sinusoid mazework Sinusichnus sinuosus, and the boxwork bag-like trace consisting of highly symmetric horizontal galleries and numerous semi-equidistant vertical shafts. The occurrence of these complex trace fossils suggests distinct behavioural complication and novelty in deep-sea communities during the Middle–Late Ordovician. We speculate that along with the onshore–offshore displacement of ichnofauna and significant expansion of deposit-feeding structures possibly driven by accelerated competition in the shallow-marine niches and aided by ameliorated deep-sea benthic food level, there was underlying behavioural evolution towards more delicate, geometric, and efficient feeding patterns. The Late Ordovician may represent the early peak not only in ichnodiversity but also in ichnodisparity and behavioural complexity of deep-sea ichnofauna, which probably reflect the complex interplay of biodiversity, biomass, and ecological changes during the Ordovician Radiation.

Staining and Tracking Methods for Studying Sponge Cell Dynamics.

To better understand the origin of animal cell types, body plans, and other morphological features, further biological knowledge and understanding are needed from non-bilaterian phyla, namely, Placozoa, Ctenophora, and Porifera. This chapter describes recent cell staining approaches that have been developed in three phylogenetically distinct sponge species-the homoscleromorph Oscarella lobularis, and the demosponges Amphimedon queenslandica and Lycopodina hypogea-to enable analyses of cell death, proliferation, and migration. These methods allow for a more detailed understanding of cellular behaviors and fates, and morphogenetic processes in poriferans, building on current knowledge of sponge cell biology that relies chiefly on classical (static) histological observations.

The Diversity of Muscles and Their Regenerative Potential across Animals.

Cells with contractile functions are present in almost all metazoans, and so are the related processes of muscle homeostasis and regeneration. Regeneration itself is a complex process unevenly spread across metazoans that ranges from full-body regeneration to partial reconstruction of damaged organs or body tissues, including muscles. The cellular and molecular mechanisms involved in regenerative processes can be homologous, co-opted, and/or evolved independently. By comparing the mechanisms of muscle homeostasis and regeneration throughout the diversity of animal body-plans and life cycles, it is possible to identify conserved and divergent cellular and molecular mechanisms underlying muscle plasticity. In this review we aim at providing an overview of muscle regeneration studies in metazoans, highlighting the major regenerative strategies and molecular pathways involved. By gathering these findings, we wish to advocate a comparative and evolutionary approach to prompt a wider use of “non-canonical” animal models for molecular and even pharmacological studies in the field of muscle regeneration.

The 'biomineralization toolkit' and the origin of animal skeletons.

Biomineralized skeletons are widespread in animals, and their origins can be traced to the latest Ediacaran or early Cambrian fossil record, in virtually all animal groups. The origin of animal skeletons is inextricably linked with the diversification of animal body plans and the dramatic changes in ecology and geosphere-biosphere interactions across the Ediacaran-Cambrian transition. This apparent independent acquisition of skeletons across diverse animal clades has been proposed to have been driven by co-option of a conserved ancestral genetic toolkit in different lineages at the same time. This 'biomineralization toolkit' hypothesis makes predictions of the early evolution of the skeleton, predictions tested herein through a critical review of the evidence from both the fossil record and development of skeletons in extant organisms. Furthermore, the distribution of skeletons is here plotted against a time-calibrated animal phylogeny, and the nature of the deep ancestors of biomineralizing animals interpolated using ancestral state reconstruction. All these lines of evidence point towards multiple instances of the evolution of biomineralization through the co-option of an inherited organic skeleton and genetic toolkit followed by the stepwise acquisition of more complex skeletal tissues under tighter biological control. This not only supports the 'biomineralization toolkit' hypothesis but also provides a model for describing the evolution of complex biological systems across the Ediacaran-Cambrian transition.

Evolutionary Diversity of the Mechanisms Providing the Establishment of Left-Right Asymmetry in Metazoans

Left-right asymmetry is an important feature of the body plan of bilaterian animals. Malformations of the left-right axis result in pathologies of varying severity. Therefore, studying the mechanisms of its establishment in embryonic development is important for science and medicine. The main question to answer in the course of research is how and when the symmetry breakage in a developing organism occurs. This area of research is intensely developing, and various mechanisms of the left-right axis establishment have already been discovered in animals of different phylogenetic groups. Unfortunately, comparative studies of these mechanisms often focus on a few phylogenetically distant objects of developmental biology and do not analyze the diversity that exists within the taxonomic groups. Therefore, the aims of this review are to show the diversity of mechanisms for establishing left-right asymmetry in the early development of metazoans, to make assumptions about the evolutionary conservatism of these mechanisms, and to establish which of the mechanisms is primary for the Bilateria and for the Metazoa in general. The article systematizes our knowledge about the establishment of left-right asymmetry on the basis of the Nodal signaling cascade activity, compares the morphology and functioning of the left-right organizers of different animals, and compares the role of mechanical tensions in establishing asymmetry in different Protostomia. Generalization and analysis of data on the establishment of left-right asymmetry provides a new insight into the evolution of the development of metazoans.

The origin of animal body plans: a view from fossil evidence and the regulatory genome.

The origins and the early evolution of multicellular animals required the exploitation of holozoan genomic regulatory elements and the acquisition of new regulatory tools. Comparative studies of metazoans and their relatives now allow reconstruction of the evolution of the metazoan regulatory genome, but the deep conservation of many genes has led to varied hypotheses about the morphology of early animals and the extent of developmental co-option. In this Review, I assess the emerging view that the early diversification of animals involved small organisms with diverse cell types, but largely lacking complex developmental patterning, which evolved independently in different bilaterian clades during the Cambrian Explosion.

Assaying Chromatin Accessibility Using ATAC-Seq in Invertebrate Chordate Embryos.

Cis-regulatory elements (CREs) are non-coding DNA regions involved in the spatio-temporal regulation of gene expression. Gene regulatory changes drive animal development and play major roles during evolution of animal body plans. Therefore, we believe that determining CREs at different developmental stages and across animal lineages is critical to understand how evolution operates through development. The Assay for Transposase-Accessible Chromatin followed by high-throughput sequencing (ATAC-seq) is a powerful technique for the study of CREs that takes advantage of Tn5 transposase activity. Starting from fewer than 105 cells, in a 1-day procedure, it is possible to detect, at a genome-wide level, CREs located in open chromatin regions with high resolution. Here, we describe a detailed step-by-step ATAC-seq protocol for invertebrate chordate marine embryos. We have successfully applied this technique to amphioxus and two species of tunicate embryos. We also show an easy workflow to analyze data generated with this technique. Moreover, we point out that this method and our bioinformatic pipeline are efficient to detect CREs associated with Wnt signaling pathway by simply using embryos treated with a drug that perturbs this pathway. This approach can be extended to other signaling pathways and also to embryo mutants for critical genes. Our results therefore demonstrate the power of ATAC-seq for the identification of CREs that play essential functions during animal development in a wide range of invertebrate or vertebrate animals.

Cellular, molecular, and biophysical control of epithelial cell intercalation.

Convergent extension is a conserved mechanism for elongating tissues. In the Drosophila embryo, convergent extension is driven by planar polarized cell intercalation and is a paradigm for understanding the cellular, molecular, and biophysical mechanisms that establish tissue structure. Studies of convergent extension in Drosophila have provided key insights into the force-generating molecules that promote convergent extension in epithelial tissues, as well as the global systems of spatial information that systematically organize these cell behaviors. A general framework has emerged in which asymmetrically localized proteins involved in cytoskeletal tension and cell adhesion direct oriented cell movements, and spatial signals provided by the Toll, Tartan, and Teneurin receptor families break planar symmetry to establish and coordinate planar cell polarity throughout the tissue. In this chapter, we describe the cellular, molecular, and biophysical mechanisms that regulate cell intercalation in the Drosophila embryo, and discuss how research in this system has revealed conserved biological principles that control the organization of multicellular tissues and animal body plans.

Lighting up the central dogma for predictive developmental biology.

Although the last 30years have witnessed the mapping of the wiring diagrams of the gene regulatory networks that dictate cell fate and animal body plans, specific understanding building on such network diagrams that shows how DNA regulatory regions control gene expression lags far behind. These networks have yet to yield the predictive power necessary to, for example, calculate how the concentration dynamics of input transcription factors and DNA regulatory sequence prescribes output patterns of gene expression that, in turn, determine body plans themselves. Here, we argue that reaching a predictive understanding of developmental decision-making calls for an interplay between theory and experiment aimed at revealing how the regulation of the processes of the central dogma dictate network connections and how network topology guides cells toward their ultimate developmental fate. To make this possible, it is crucial to break free from the snapshot-based understanding of embryonic development facilitated by fixed-tissue approaches and embrace new technologies that capture the dynamics of developmental decision-making at the single cell level, in living embryos.