Evolutionary origin of the chordate nervous system revealed by amphioxus developmental trajectories.

The common ancestor of all vertebrates had a highly sophisticated nervous system, but questions remain about the evolution of vertebrate neural cell types. The amphioxus, a chordate that diverged before the origin of vertebrates, can inform vertebrate evolution. Here we develop and analyse a single-cell RNA-sequencing dataset from seven amphioxus embryo stages to understand chordate cell type evolution and to study vertebrate neural cell type origins.

A microfluidic chip for immobilization and imaging of Ciona intestinalis larvae.

Sea squirts (Tunicata) are chordates and develop a swimming larva with a small and defined number of individually identifiable cells. This offers the prospect of connecting specific stimuli to behavioral output and characterizing the neural activity that links these together. Here, we describe the development of a microfluidic chip that allows live larvae of the sea squirt Ciona intestinalis to be immobilized and recorded.

Amphioxus knockout disrupts the development of left-right asymmetry but has limited impact on neural patterning.

Unlabelled: The Gli transcription factors are the primary mediators of Hedgehog (Hh) signaling. Vertebrate genomes contain multiple paralogues with different functions downstream of Hh signal receipt, in part explaining the complexity of cellular responses to Hh that allow concentration-dependent target gene activation. Amphioxus is a chordate that split from the vertebrate lineage early in the evolution of chordates, before the genome duplications that occurred in early vertebrate evolution.

Evolution of the expression and regulation of the nuclear hormone receptor ERR gene family in the chordate lineage.

The Estrogen Related Receptor (ERR) nuclear hormone receptor genes have a wide diversity of roles in vertebrate development. In embryos, ERR genes are expressed in several tissues, including the central and peripheral nervous systems. Here we seek to establish the evolutionary history of chordate ERR genes, their expression and their regulation.

Hmx gene conservation identifies the origin of vertebrate cranial ganglia.

The evolutionary origin of vertebrates included innovations in sensory processing associated with the acquisition of a predatory lifestyle. Vertebrates perceive external stimuli through sensory systems serviced by cranial sensory ganglia, whose neurons arise predominantly from cranial placodes; however, the understanding of the evolutionary origin of placodes and cranial sensory ganglia is hampered by the anatomical differences between living lineages and the difficulty in assigning homology between cell types and structures. Here we show that the homeobox transcription factor Hmx is a constitutive component of vertebrate sensory ganglion development and that in the tunicate Ciona intestinalis, Hmx is necessary and sufficient to drive the differentiation programme of bipolar tail neurons, cells previously thought to be homologues of neural crest.

Extensive non-redundancy in a recently duplicated developmental gene family.

Background: It has been proposed that recently duplicated genes are more likely to be redundant with one another compared to ancient paralogues. The evolutionary logic underpinning this idea is simple, as the assumption is that recently derived paralogous genes are more similar in sequence compared to members of ancient gene families. We set out to test this idea by using molecular phylogenetics and exploiting the genetic tractability of the model nematode, Caenorhabditis elegans, in studying the nematode-specific family of Hedgehog-related genes, the Warthogs.

The evolutionary origins of the vertebrate olfactory system.

Vertebrates develop an olfactory system that detects odorants and pheromones through their interaction with specialized cell surface receptors on olfactory sensory neurons. During development, the olfactory system forms from the olfactory placodes, specialized areas of the anterior ectoderm that share cellular and molecular properties with placodes involved in the development of other cranial senses. The early-diverging chordate lineages amphioxus, tunicates, lampreys and hagfishes give insight into how this system evolved.

Step-wise evolution of neural patterning by Hedgehog signalling in chordates.

In vertebrate embryos, Hedgehog (Hh) is expressed in some anterior basal plate domains and by notochord and floorplate cells, and ventral neural cells are patterned by the activities of Hh-regulated transcription factors. Hh signalling is antagonized by signals from the dorsal neural tube and loss of Hh leads to loss of ventral patterning as dorsal pattern expands. These mechanisms are critical for producing the neurons that implement motor responses to sensory inputs but understanding how they evolved has been hindered by lack of insight from commonly studied invertebrates where nervous system morphology and genetic mechanisms are non-conserved with vertebrates.

Evolution of vertebrate spinal cord patterning.

The vertebrate spinal cord is organized across three developmental axes, anterior-posterior (AP), dorsal-ventral (DV), and medial-lateral (ML). Patterning of these axes is regulated by canonical intercellular signaling pathways: the AP axis by Wnt, fibroblast growth factor, and retinoic acid (RA), the DV axis by Hedgehog, Tgfβ, and Wnt, and the ML axis where proliferation is controlled by Notch. Developmental time plays an important role in which signal does what and when.

Live Imaging of Cleavage Variability and Vesicle Flow Dynamics in Dextral and Sinistral Spiralian Embryos.

Spiral cleavage is a mode of embryonic cell division found in species from several Phyla, including molluscs, annelids and flatworms. It reflects a tilting in the direction of spindle orientation and cell division at the 4 to 8-cell stage, which may be dextral or sinistral, and propagates into later organismal asymmetry. Genetic analysis in a small number of gastropod molluscs shows the direction of spiral cleavage is determined by maternal genotype, though whether this is also the case more generally for spiralians, and whether spiral cleavage at the 4-8 cell stage is preceded by earlier internal chirality in any spiralian species, is unknown.

DnaJ chaperones contribute to canalization.

Canalization, an intrinsic robustness of development to external (environmental) or internal (genetic) perturbations, was first proposed over half a century ago. However, whether the robustness to environmental stress (environmental canalization [EC]) and to genetic variation (genetic canalization) are underpinned by the same molecular basis remains elusive. The recent discovery of the involvement of two endoplasmic reticulum (ER)-associated DnaJ genes in developmental buffering, orthologues of which are conserved across Metazoa, indicates that the role of ER-associated DnaJ genes might be conserved across the animal kingdom.

A Notch-regulated proliferative stem cell zone in the developing spinal cord is an ancestral vertebrate trait.

Vertebrates have evolved the most sophisticated nervous systems we know. These differ from the nervous systems of invertebrates in several ways, including the evolution of new cell types, and the emergence and elaboration of patterning mechanisms to organise cells in time and space. Vertebrates also generally have many more cells in their central nervous systems than invertebrates, and an increase in neural cell number may have contributed to the sophisticated anatomy of the brain and spinal cord.

Developmental signature, synaptic connectivity and neurotransmission are conserved between vertebrate hair cells and tunicate coronal cells.

In tunicates, the coronal organ represents a sentinel checking particle entrance into the pharynx. The organ differentiates from an anterior embryonic area considered a proto-placode. For their embryonic origin, morphological features and function, coronal sensory cells have been hypothesized to be homologues to vertebrate hair cells.

The structure, splicing, synteny and expression of lamprey COE genes and the evolution of the COE gene family in chordates.

COE genes encode transcription factors that have been found in all metazoans examined to date. They possess a distinctive domain structure that includes a DNA-binding domain (DBD), an IPT/TIG domain and a helix-loop-helix (HLH) domain. An intriguing feature of the COE HLH domain is that in jawed vertebrates it is composed of three helices, compared to two in invertebrates.

Phylogenetics of Lophotrochozoan bHLH Genes and the Evolution of Lineage-Specific Gene Duplicates.

The gain and loss of genes encoding transcription factors is of importance to understanding the evolution of gene regulatory complexity. The basic helix-loop-helix (bHLH) genes encode a large superfamily of transcription factors. We systematically classify the bHLH genes from five mollusc, two annelid and one brachiopod genomes, tracing the pattern of bHLH gene evolution across these poorly studied Phyla.

Cerberus-Nodal-Lefty-Pitx signaling cascade controls leftright asymmetry in amphioxus.

Many bilaterally symmetrical animals develop genetically programmed left-right asymmetries. In vertebrates, this process is under the control of Nodal signaling, which is restricted to the left side by antagonists Cerberus and Lefty. Amphioxus, the earliest diverging chordate lineage, has profound left-right asymmetry as a larva.

Identification of genes for engineering the male germline of Aedes aegypti and Ceratitis capitata.

Background: Synthetic biology approaches are promising new strategies for control of pest insects that transmit disease and cause agricultural damage. These strategies require characterised modular components that can direct appropriate expression of effector sequences, with components conserved across species being particularly useful. The goal of this study was to identify genes from which new potential components could be derived for manipulation of the male germline in two major pest species, the mosquito Aedes aegypti and the tephritid fruit fly Ceratitis capitata.

Insect transformation with piggyBac: getting the number of injections just right.

The insertion of exogenous genetic cargo into insects using transposable elements is a powerful research tool with potential applications in meeting food security and public health challenges facing humanity. piggyBac is the transposable element most commonly utilized for insect germline transformation. The described efficiency of this process is variable in the published literature, and a comprehensive review of transformation efficiency in insects is lacking.

Identification of molecular signatures specific for distinct cranial sensory ganglia in the developing chick.

Background: The cranial sensory ganglia represent populations of neurons with distinct functions, or sensory modalities. The production of individual ganglia from distinct neurogenic placodes with different developmental pathways provides a powerful model to investigate the acquisition of specific sensory modalities. To date there is a limited range of gene markers available to examine the molecular pathways underlying this process.

Molecular basis of canalization in an ascidian species complex adapted to different thermal conditions.

Canalization is a result of intrinsic developmental buffering that ensures phenotypic robustness under genetic variation and environmental perturbation. As a consequence, animal phenotypes are remarkably consistent within a species under a wide range of conditions, a property that seems contradictory to evolutionary change. Study of laboratory model species has uncovered several possible canalization mechanisms, however, we still do not understand how the level of buffering is controlled in natural populations.

Draft genome assemblies and predicted microRNA complements of the intertidal lophotrochozoans Patella vulgata (Mollusca, Patellogastropoda) and Spirobranchus (Pomatoceros) lamarcki (Annelida, Serpulida).

MicroRNAs (miRNA) are small non-coding RNAs that act post-transcriptionally to regulate gene expression levels. Some studies have indicated that microRNAs may have low homoplasy, and as a consequence the phylogenetic distribution of microRNA families has been used to study animal evolutionary relationships. Limited levels of lineage sampling, however, may distort such analyses.

Transmission and Scanning Electron Microscopy of the Accessory Cells and Chorion During Development of Ciona intestinalis Type B Embryos and the Impact of Their Removal on Cell Morphology.

Spawned ascidian oocytes are surrounded by a membrane called the chorion (or vitelline coat) and associated with two populations of maternally-supplied cells. Outside the chorion are follicle cells, which may affect the buoyancy of eggs. Inside the chorion are test cells, which during oogenesis provision the egg and which after fertilisation contribute to the larval tunic.

Characterization of two neurogenin genes from the brook lamprey lampetra planeri and their expression in the lamprey nervous system.

Conclusions: Neurogenins are required for the specification of neuronal precursors and regulate the expression of basic Helix-Loop-Helix genes involved in neuronal differentiation. Jawed vertebrates possess three Neurogenin paralogy groups and their combined expression covers the entire nervous system, apart from the autonomic nervous system.

Results: Here we report the isolation of two Neurogenin genes, LpNgnA and LpNgnB, from the lamprey Lampetra planeri.

The Lophotrochozoan TGF-β signalling cassette - diversification and conservation in a key signalling pathway.

TGF-β signalling plays a key role in the patterning of metazoan body plans and growth. It is widely regarded as a 'module' capable of co-option into novel functions. The TGF-β pathway arose in the Metazoan lineage, and while it is generally regarded as well conserved across evolutionary time, its components have been largely studied in the Ecdysozoa and Deuterostomia.

Symmetrical reproductive compatibility of two species in the Ciona intestinalis (Ascidiacea) species complex, a model for marine genomics and developmental biology.

The sea squirt Ciona intestinalis species complex is a widely used model system for genomics and developmental biology, as well as ecology. Contrary to previous reports, here we show no difference in the success of development and hatching between hybrid and conspecific crosses between the two species within this complex known as types A and B, from a region in the English Channel where they are sympatric. We grew laboratory hybrids in the field for three months, and successfully obtained reproductive adults.