The bilaterian forebrain: an evolutionary chimaera

Tosches, Maria Antonietta; Arendt, Detlev

doi:10.1016/j.conb.2013.09.005

Cited by 83 publications

(101 citation statements)

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“…The former is neurosecretory and the latter involves motor centers. These two systems fused to form a forebrain in the bilaterian ancestor (Tosches and Arendt, 2013). A final scheme is that the deuterostome ancestor had parallel five nerve cords and an anterior brain, and these nerve cords evolved into the radial nerves of echinoderms (Kuznetsov, 2012).…”

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Evolution of basal deuterostome nervous systems

Holland

2015

Journal of Experimental Biology

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Understanding the evolution of deuterostome nervous systems has been complicated by the ambiguous phylogenetic position of the Xenocoelomorpha (Xenoturbellids, acoel flat worms, nemertodermatids), which has been placed either as basal bilaterians, basal deuterostomes or as a sister group to the hemichordate/ echinoderm clade (Ambulacraria), which is a sister group of the Chordata. None of these groups has a single longitudinal nerve cord and a brain. A further complication is that echinoderm nerve cords are not likely to be evolutionarily related to the chordate central nervous system. For hemichordates, opinion is divided as to whether either one or none of the two nerve cords is homologous to the chordate nerve cord. In chordates, opposition by two secreted signaling proteins, bone morphogenetic protein (BMP) and Nodal, regulates partitioning of the ectoderm into central and peripheral nervous systems. Similarly, in echinoderm larvae, opposition between BMP and Nodal positions the ciliary band and regulates its extent. The apparent loss of this opposition in hemichordates is, therefore, compatible with the scenario, suggested by Dawydoff over 65 years ago, that a true centralized nervous system was lost in hemichordates. KEY WORDS: Cephalochordate, Deuterostomes, Echinoderm, Hemichordate, Nervous system evolution IntroductionDeuterostomes include at least the Chordata (vertebrates, tunicates and cephalochordates) and the Ambulacraria (echinoderms and hemichordates). The enigmatic Xenoturbellida has been placed either basally in the deuterostomes or together with acoel flatworms as the Xenocoelomorpha -the sister group of the Ambulacraria. Alternatively, the Xenocoelomorpha have been placed basal to the bilateria (reviewed in Achatz et al., 2013). Xenoturbella has a very simple body plan with a nerve net and is thought to have lost a number of ancestral features (Philippe et al., 2011). Therefore, it is unclear whether it is at all relevant to the evolution of deuterostome nervous systems. However, there is no question that echinoderms and hemichordates are deuterostomes. In most phylogenetic analyses, Ambulacraria are the sister group of the chordates (Blair and Hedges, 2005; Delsuc et al., 2008; Edgecombe et al., 2011). However, a recent analysis based on 586 nuclear genes places cephalochordates as the sister group of the Ambulacraria with high bootstrap support and cephalochordates plus Ambulacraria as the sister group of tunicates plus vertebrates (Moroz et al., 2014). Because the nervous systems of echinoderms, hemichordates and chordates are so very different, it has been controversial whether the ancestral deuterostome had a longitudinal nerve cord or a nerve net or a combination of both.Several schemes for the evolution of deuterostome nervous systems have focused on the possible contribution of the larval REVIEW Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, USA.*Author for correspondence (lzholland@ucsd.edu)...

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Evolution of basal deuterostome nervous systems

Holland

2015

Journal of Experimental Biology

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“…The apical organ consists of a group of columnar or flask-shaped cells usually with one cilium, but in some species with several; it does not fit the narrow definition of a ganglion, because it apparently comprises only sensory cells (Richter et al, 2010). Many spiralians develop lateral (cerebral) ganglia in close apposition to the apical organ, and this compound structure has been called the apical organ in most of the older morphological literature, and this is also seen in some studies on gene expression (Tosches and Arendt, 2013). However, most recent papers use the term apical organ in the restricted sense in accordance with the terminology of Richter et al (Richter et al, 2010).…”

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Larval nervous systems: true larval and precocious adult

Nielsen

2015

Journal of Experimental Biology

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The apical organ of ciliated larvae of cnidarians and bilaterians is a true larval organ that disappears before or at metamorphosis. It appears to be sensory, probably involved in metamorphosis, but knowledge is scant. The ciliated protostome larvae show ganglia/nerve cords that are retained as the adult central nervous system (CNS). Two structures can be recognized, viz. a pair of cerebral ganglia, which form the major part of the adult brain, and a blastoporal (circumblastoporal) nerve cord, which becomes differentiated into a perioral loop, paired or secondarily fused ventral nerve cords and a small perianal loop. The anterior loop becomes part of the brain. This has been well documented through cell-lineage studies in a number of spiralians, and homologies with similar structures in the ecdysozoans are strongly indicated. The deuterostomes are generally difficult to interpret, and the nervous systems of echinoderms and enteropneusts appear completely enigmatic. The ontogeny of the chordate CNS can perhaps be interpreted as a variation of the ontogeny of the blastoporal nerve cord of the protostomes, and this is strongly supported by patterns of gene expression. The presence of 'deuterostomian' blastopore fates both in an annelid and in a mollusk, which are both placed in families with the 'normal' spiralian gastrulation type, and in the chaetognaths demonstrates that the chordate type of gastrulation could easily have evolved from the spiralian type. This indicates that the latest common ancestor of the deuterostomes was very similar to the latest common pelago-benthic ancestor of the protostomes as described by the trochaea theory, and that the neural tube of the chordates is morphologically ventral. KEY WORDS: Deuterostomy, Metamorphosis, Nervous systems, Dorsal-ventral orientation IntroductionStudies on ontogeny are very important for our understanding of nervous system evolution and diversification, and new methods have made important contributions to knowledge of the structure and development of larval nervous systems and their relationships to adult nervous systems.The nervous system has for a long time been considered one of the most conservative animal organ systems and has therefore been given high importance in studies of animal evolution. More than a century ago, Hatschek (Hatschek, 1888) introduced the names Zygoneura (now Protostomia), Ambulacraria and Chordonia (now Chordata) for three major groups of the Bilateria, based on the structure and position of the central nervous system (CNS). The Zygoneura were characterized by a paired longitudinal ventral nerve cord [a cluster of nervous cells including their cell bodies, as opposed to a nerve, which is a bundle of axons (Richter et al., 2010); the ventral nerve cord may REVIEWThe Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.*Author for correspondence (cnielsen@snm.ku.dk) be specialized into rows of ganglia connected by connectives] and the Chordonia by an unpaired dorsal n...

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“…Such organisation occurred with the emergence of borders between brain domains, such as the midbrain/hindbrain boundary. Recently, following studies in an annelid worm, Arendt and colleagues proposed that the nervous system of the common bilaterian ancestor was probably composed of two independent domains (corresponding to the vertebrate forebrain/midbrain and hindbrain) that later fused during evolution (Tosches and Arendt 2013).…”

Section: A Short Natural History Of the Nervous System: Several Questmentioning

confidence: 99%

Aquatic Model Organisms in Neurosciences: The Genome-Editing Revolution

Joly¹

2017

Research and Perspectives in Neurosciences

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The use of aquatic model organisms has been greatly diversified in laboratories. Zebrafish is the most advanced aquatic species for the use of Crispr-Cas9 in laboratories. Because of the simplicity and broad applicability of this later system, knock-out is now efficiently performed at medium scale. Forward genetics in zebrafish can now be performed by CRISPR-based F0 screening using high speed and high content phenotyping for example by confocal imaging. As zebrafish, marine model organisms have the prominent advantage to be transparent, all the more at young stages (embryos and larvae) or when fixed samples are cleared by novel methods. The Cripsr-Cas9 system is routinely used in the ascidian Ciona intestinalis. It also starts to be used in many other marine models, such as the medusa Clythia hemispherica. We provide at the end of this review a list of aquatic model species and some examples of questions on the origin of our nervous system that can be coped with these models, where the possibility to perform genome editing would constitute a major advance.

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The bilaterian forebrain: an evolutionary chimaera

Cited by 83 publications

References 102 publications

Evolution of basal deuterostome nervous systems

Evolution of basal deuterostome nervous systems

Larval nervous systems: true larval and precocious adult

Aquatic Model Organisms in Neurosciences: The Genome-Editing Revolution

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