Origin and evolution of the nervous system

The origins and early evolution of animals and their nervous systems

Professor Graham Budd, Uppsala University, Sweden

Abstract

Nervous systems evolved as early animals started to encounter (and generate) increasingly heterogeneous spatial and ecological environments. It is clear that the earliest stages of this process took place in the Precambrian (> 540 Ma), although I shall argue that there are no deep roots to complex animals before about 585 Ma. If so, the enigmatic Ediacaran assemblages should provide crucial clues to the origins of modern complex diversity. Interpretation of this early record is partly dependent on, as yet, controverted phylogenies of extant organisms. Nevertheless, I shall argue that the roots of animal diversity lie within these assemblages. Bilaterality and mobility seem to be key correlative factors in complex nervous system organisation, and the possible correlated progression of these features through the Precambrian-Cambrian boundary will be explored. The subtle interplay between behaviour and behavioural possibilities provided a critical framework within which early nervous system evolution took place. In the Cambrian, the appearance of recognisable clades (in particular the arthropods) allows more concrete conclusions to be drawn about early nervous system evolution. Although great progress has been made in understanding the evolution of (especially) early arthropod nervous systems, continued uncertainty in upper stem-group arthropod phylogeny is hampering the tracing of the complete history of the arthropod brain.

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Cambrian brains: their occurrence and significance for systematics

Dr Greg Edgecombe, Natural History Museum, UK

Abstract

Extant panarthropods are hallmarked by stunning morphological and taxonomic diversity but their central nervous systems are relatively conserved. The timing of divergences of the groundplan CNS organisation of Onychophora, Tardigrada, Chelicerata and Mandibulata has been poorly constrained because of a scarcity of data from the early fossil record. Although CNS has been documented in three-dimensional detail in insects from Cenozoic ambers, it is widely assumed that these tissues are too prone to decay to withstand other styles of fossilisation or geologically older preservation.  However, Cambrian Burgess Shale-type Konservat Lagerstätten – notably the Chengjiang and Xiaoshiba biotas (China) and the Burgess Shale (Canada) – have emerged as sources of fossilised brains and nerve cords, as well as structural details of the eyes and the distributions of sensilla. CNS in these Cambrian compression fossils is replicated by iron oxides/hydroxides after pyrite or is preserved as carbon films. The brain of the putative stem-group euarthropod Fuxianhuia exhibits a tripartite organisation comparable to crown-group mandibulates, whereas neural characters of the Cambrian megacheiran Alalcomenaeus reinforce chelicerate affinities of “great appendage” arthropods. CNS and compound eye characters predict divergences of the mandibulate and chelicerate groundpatterns by the early Cambrian, ca 518 Ma. Deeper in the euarthropod stem, anomalocaridids possess apposition optics and paired preocular ganglia in association with the brain. Experiments with carcasses compacted in fine-grained sediment challenge the expectation that the CNS is too labile to withstand the temporal window for early diagenetic mineralisation.

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Early metazoan life: divergence, environment and ecology

Dr Douglas Erwin, National Museum of Natural History, USA

Abstract

Most recent molecular clock studies suggest the origin of metazoa dates to about 750-800Ma, which is also consistent with recent evidence from geochemical proxies that oxygen levels increased from <0.1% PAL to perhaps 1-3% PAL O2.  The primary alternative to this would involve greatly increased substitution rates across many clades and many genes; while not impossible this is a less parsimonious reading of the data. Yet the first reliable fossil evidence for metazoans is about 600 (the Duoshantuo embryos), followed by the Ediacaran fossils after 580 Ma with the earliest undisputed bilaterians at 555 Ma, and an increase in the size and morphologic complexity of bilaterians around 542 Ma. This temporal framework suggests a missing 150-200 Ma of early metazoan divergence that encompasses many of the interesting things associated with the early evolution of the nervous system. This span including two major glaciations, the development complex geochemical changes in the oceans, including major changes in redox, and other environmental changes. To a first approximation, origins of most of the major features of metazoan body plans, including the nervous system, was accomplished during the Cryogenian and Ediacaran. I will provide a summary of the timing of the major novelties in the invention of the nervous system within the context of the metazoan divergences and environmental changes from 800 to 530 Ma.

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Chair

Dr Paul Katz, Georgia State University, USA

Introduction to the “Origin and evolution of the nervous system”

Professor Nicholas Strausfeld FRS, University of Arizona, USA
Dr Frank Hirth, King's College London, UK

Abstract

In his great work Micrographia published by the Royal Society in 1665, Robert Hooke demonstrated both the power of the microscope, his wonderful novelty, and his gift for comparative observations, one of which explained that despite their differences the compound eyes of arthropods and the single lens eyes of vertebrates must be organised to similarly perceive the visual world. Although Hooke heralded the discipline of comparative observation it was not until 1818 that Étienne Geoffroy Saint-Hilaire made the startling proposal that the nervous systems of arthropods and vertebrates, although inverted, were analogous and derived from a single plan of organisation. His compatriot, the anatomist Georges Cuvier, argued that organisms are naturally grouped into four embranchments, unrelated and unchanged over time. Their public debate at the Académie Royale des Sciences in Paris in 1830, caused a public furore but remained unresolved. Today molecular genetics and genomics reignite the Académie debate, revealing genetic mechanisms acting not only to specify dorso-ventral and anterior-posterior axes but showing too that segmentation, neurogenesis, and axogenesis appear to be conserved across much of the animal kingdom. Congruence between genetic and geological fossil records suggests that already by the “Cambrian explosion” arthropods and chordates shared a genealogically corresponding brain organisation. This summary provides the background context for this meeting, which will consider the origin and evolution of nervous systems, integrating knowledge ranging from evolutionary theory and palaeontology to comparative developmental genetics and phylogenomics, thereby allowing evidence-based debates for and against the proposition that brains and nervous systems derive from a common ancestor.

• Speaker audio recording - Nicholas Strausfeld (mp3)
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Cnidaria and the emergence of neurogenesis

Professor Brigitte Galliot, University of Geneva, Switzerland

Abstract

Hydra is a freshwater cnidarian polyp formed of two epithelial cell layers and three stem cell populations, equipped with a sophisticated apical nervous system that includes sensory-motor neurons, ganglia neurons and mechano-sensory cells named nematocytes. All these cells differentiate from interstitial stem cells, and are continuously replaced all along the life of the animals, highlighting the extreme dynamism of neurogenesis in Hydra. Previous studies also showed that animals easily survive the drug- or heatshock-induced elimination of interstitial stem cells that leave the epithelial cells unaffected. Several weeks later such Hydra become “epithelial”, i.e. have lost all their nerve cells, no longer react to touch nor catch their food, but surprisingly still regenerate after bisection, or bud when force-fed. However, Hydra oligactis that can undergo aging, rapidly loose de novo neurogenesis in this context, with dramatic impact on their neurological and developmental behaviours. To assess the role of adult de novo neurogenesis in the maintenance of fitness, regeneration and senescence, we performed quantitative RNAseq analysis on intact, heat-shocked, Hydroxyurea-treated or aging Hydra. We will present and discuss the obtained results in light of evolutionary considerations.

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Chair

Dr Erich Jarvis, Duke University and Howard Hughes Medical Institute, USA

An option space for early neural evolution

Dr Gáspár Jékely, Living Systems Institute, University of Exeter, UK

Abstract

The origin of nervous systems has traditionally been discussed within two conceptual frameworks. Input-output models stress the sensory-motor aspects of nervous systems, while internal coordination models emphasise the role of nervous systems in coordinating large-scale body movements. Here we consider both frameworks and apply them to describe aspects of each of three main groups of phenomena that nervous systems control: behaviour, physiology and development. We argue that both frameworks and all three aspects of nervous system function need to be considered for a comprehensive discussion of nervous system origins. This broad mapping of the option space enables a more comprehensive overview of the many influences and constraints that may have played a role in the evolution of the first nervous systems.

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Genomic bases of multiple origins and parallel evolution of neurons and synapses: insights from ctenophores and molluscs

Professor Leonid Moroz, University of Florida, USA

Abstract

Advances in Omics and their implementations to basal metazoan clades (Ctenophora, Porifera, Placozoa, Cnidaria, Bilateria) resulted to revisions of the animal phylogeny and hypotheses of neural evolution. Our analysis suggests that both neurons and synapses evolved independently from different cell lineages recruiting the ancestral machinery for secretion and reception developed in early eukaryotes.

The first case is the independent origin of neurons in ctenophores as evidenced by our combined genomic, proteomic, metabolomics and physiological studies on four ctenophore species (Pleurobrachia, Mnemiopsis, Bolinopsis and Beroe). Historically, temporal differentiation of cellular phenotypes found in unicellular eukaryotes (as result of their complex life cycles) was substituted and extended by spatial differentiation in metazoans leading to a greater diversity of cell types. Some components of synaptic and neuronal machinery might represent examples of convergent evolution.   

The second remarkable example is the parallel origins of cell lineages supporting intercellular signaling using various transmitters. Combining data from 10+ phyla, including single-neuron RNA-seq and, unbiased single-cell epigenomic profiling, we will discuss how recruitment of various molecular modules together with environmental constrains might lead to independent origins of neurons and synapses across distinct animal clades.

Phylogenetic reconstructions also suggest that neuronal centralisation and mosaic formation of complex brains evolved at least 12 times across the animal kingdom, with 5 independent centralisation events in the molluscan clade including cephalopods - the ‘primates of the sea’. Thus, we define neurons as a functional rather than a genetic category. Neurons are polarised secretory cells specialised for directional propagation of electrical signals leading to release of intracellular messengers – features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbours without affecting all intervening cells en route. However, using an array of molecular markers within some animal lineages, especially in molluscs, one can recognise homologous neuronal lineages. These examples and criteria for homologisation of distinct cell lineages will be discussed toward reconstruction of natural classification of neurons or NeuroSystematics.

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Where is my mind? How sponges and placozoans may have lost neural cell types

Dr Joseph Ryan, University of Florida, USA

Abstract

For over 150 years, it was thought that sponges were the sister group to all other animals (if they were animals at all) and that the sponge body plan represented a primitive stage in animal evolution. Similarly, it has long been thought that placozoans represent a basic body type that has endured hundreds of million years of evolution. Recent phylogenetic analyses of animal genomes and transcriptomes, however, have challenged these ideas, suggesting that ctenophores are the sister group to all other animals and implying that sophisticated cell types like neurons either evolved multiple times or were lost during the evolution of sponges and placozoans. Thus far, the far more preferred hypothesis appears to be that neural cell types evolved multiple times. I argue that historical bias may be playing a role in the rejection of cell-type loss as an explanation of the data, and that a novel analysis of evidence in light of this hypothesis is both compelling and revealing.

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Development and structure of anthozoan nervous systems

Professor Ulrich Technau, University of Vienna, Austria

Abstract

Cnidarians are the sister group of Bilateria and can therefore provide important insights into the evolution of key bilaterian traits. One of the hallmarks of bilaterians is the central nervous system. Cnidarians do not possess a central nervous system or a brain, and the nervous system of cnidarians has often been referred to as "diffuse". However, regional accumulations of neurons or nerve rings for instance found at the margin of jellyfish, as well as patterning of specific neuronal subtypes expressing different neurotransmitters suggest a certain level of complexity. Neurogenesis has been mainly studied in the hydrozoan Hydra and in the sea anemone Nematostella vectensis. While in Hydra, neurons arise from multipotent interstitial stem cells, such stem cells have not been found in Nematostella. Instead, in this organism neurons appear to differentiate directly from epithelial cells. I will discuss the similarities and differences of nervous system formation in the context of patterning of the body plan and compare it with bilaterians.

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The evolution of nervous system centralisation

Dr Detlev Arendt, European Molecular Biology Laboratory, Germany

Abstract

How animals progressed from a simple nerve net, as observed in some marine animals, to the most complex centralised nervous system, as found in humans, remains one of the most exciting and unsolved questions of animal evolution. In recent years, the molecular characterisation of neurodevelopment in a variety of marine invertebrates has yielded new insight into nervous system evolution. We are working on three animal model systems: sea anemone, amphioxus and the marine annelid Platynereis dumerilii to unravel ancestral features that existed in the cnidarian-bilaterian ancestor, the urbliaterian, or the chordate ancestor. Through this our first insights into the step-wise nervous system centralisation in divergent evolutionary lineages are beginning to emerge.

One prominent centre of early centralisation has been the ‘apical nervous system’ that played an ancient role in the modulation of activities (ciliary beating in primary larvae; muscular movements in adults) and in the general control of body physiology via the release of neuropeptides and hormones. In vertebrates the apical nervous system became incorporated into the brain. I will outline apical nervous system components in animals as diverse as amphioxus, annelids and cnidarians. 

The other centre, the ‘blastoporal nervous system’ evolved alongside the blastopore as a nerve ring around the opening of the primitive gut. A major function of this centre is the coordination of contractile movements for feeding and locomotion. I will present comparative evidence that the blastoporal nervous system has been a centre of repeated, shared as well as convergent centralisation events in both cnidarians and bilaterians.

Chair

Dr Sarah Farris, West Virginia University, USA

Developmental genes, nervous systems and reconstructing ancestors – a perspective from burrowing in the mud

Dr Chris Lowe, Stanford University, USA

Abstract

Comparative developmental biology over the past 30 years has revealed a startling level of conservation between the molecular genetic regulation of central nervous systems (CNS) between distantly related animal phyla. This has led to compelling hypotheses on the ancestry of complex bilaterian nervous systems. Much of the comparative work on body plan evolution has focused on animals defined by a complex CNS with advanced sensory and motor systems. Far less attention has been directed at animals with less complex sensory and motor systems defined by deposit or filter feeding. Enteropneust hemichordates are good representatives of these more modest neural architectures. We present detailed ectodermal patterning data during early development for two species of enteropneust with contrasting developmental modes, and demonstrate that deployment of anteroposterior patterning genes is comparable to other, more complex bilaterians. The comparative implications of these findings will be discussed in relation to the utility of molecular genetic data in reconstructing complex morphologies in deep time.

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Neurogenesis across arthropods

Dr Angelika Stollewerk, Queen Mary University of London, UK

Abstract

Arthropods represent the largest phylum in the animal kingdom and show remarkable diversity in shapes and behaviours. This raises the question of how the arthropod nervous system has evolved and been adapted to new body forms and specialised structures. Numerous studies have demonstrated a deep homology of the genetic programmes that control neurogenesis. Yet, the morphological outcome is different in each clade ranging from small numbers of neural progenitors that produce fixed lineages, to the generation of huge numbers of progenitors that generate their progeny in a seemingly random fashion. Here I discuss the different mechanisms of neurogenesis by subdividing the process into morphological and molecular modules to unravel the relation of gene function and morphological variation in the individual arthropod clades.

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Molecular clocks and nervous system evolution

Dr Gregory Wray, Duke University, USA

Abstract

Time is a critical component in understanding the grand arc of nervous system evolution. When did neurons, circuits, ganglia and brains first appear? Did independent origins of parallel traits, such as compound and cameral eyes, occur at the same time? Over what interval did dramatic transformations, such as the enormous size expansion of the human brain, take place? A rigorous temporal frame of reference allows one to address these and other interesting questions. The fossil record and molecular clocks provide the two primary (yet decidedly imperfect) sources of information available for establishing a temporal framework. Our ability to draw inferences from molecular data in particular has increased enormously during the past decade, producing more accurate estimates of some problematic but key divergence times. Combining this information with recent advances in genetics, molecular biology, and phylogenetic relationships can provide important insights into nervous system evolution. This approach will be illustrated at the broad scale of metazoan evolution and the rather narrower scale of human origins.

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Chair

Dr Heather Eisthen, Michigan State University, USA

Under the skin: how (xen-)acoelomorphs impact our understanding of nervous system evolution

Dr Andreas Hejnol, University of Bergen, Norway

Abstract

The phylogenetic position of acoelomorphs is hotly debated. Acoelomorphs are simply organised, bilateral worms that lack coeloms, segmentation and a through gut. The taxon might include the enigmatic Xenoturbella forming together the Xenacoelomorpha, which are either affiliated with the Deuterostomia or form the sister group to all remaining Bilateria. The considered positions in the animal tree of life tremendously impact the interpretation of their simple morphology: as members of Deuterostomia they are likely morphologically reduced from a more complex ancestor.  As sister-group to all remaining Bilateria, they can be seen however as ‘intermediates’ that bridge the evolution of bilaterian characters since they share characters of Cnidaria (sack-like gut) and Bilateria (bilateral symmetry, mesoderm). Despite their ambiguous phylogentic position, xenacoelomorphs have evolved novel features regarding their nervous system and are thus an ideal case for the study of the convergent evolution of brains, neurite bundles and eyes. We present data from acoels and nemertodermatids that indicate the transcription factors and signalling cascades involved in patterning acoel novelties are similar to the molecules used by bilaterians. We highlight the differences in the spatial arrangement and role of the genes in relation to the nervous system morphology and draw conclusions about the origin of the bilaterian nervous system. Conclusions for our understanding of bilaterian nervous systems are discussed.

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The origin and evolution of chordate nervous systems

Dr Linda Z. Holland, Scripps Research Institute, La Jolla, USA

Abstract

In the last 40 years, comparisons of developmental gene expression and the molecular mechanisms of development (evodevo) have joined comparative morphology as tools for reconstructing long-extinct ancestral forms. When both methods agree, the hypothetical ancestor may approximate the real one; however, both approaches typically give congruent answers only with closely related organisms. Chordate nervous systems are good examples. Everyone agrees that the ancestral chordate had a dorsal hollow nerve cord. However, morphological studies alone did not answer the question of whether the vertebrate brain was a new structure or had evolved from the anterior end of an ancestral nerve cord like that of modern amphioxus. Evodevo showed that the amphioxus brain and by extension, that of the ancestral chordate, has a diencephalic forebrain, small midbrain, hindbrain and spinal cord with parts of the genetic mechanisms in place for specifying the midbrain/hindbrain boundary, zona limitans intrathalamica and neural crest. Evodevo has also shown how extra genes resulting from two whole genome duplications at the base of the vertebrates have facilitated evolution of new structures such as neural crest. Understanding how the chordate CNS might have evolved from that of the ancestral deuterostome (i.e. the ancestor of chordates, hemichordates and echinoderms) has been especially challenging. Evidence is mounting against evolution of either larval or adult nervous systems of an ancestral echinoderm into the chordate CNS.  Two additional theories are 1) that the ancestral deuterostome had no nerve cord and that the chordate nerve cord and the two hemichordate nerve cords evolved independently and 2) that this ancestor had a CNS with a brain which gave rise to the chordate CNS and, with loss of the brain, to one of the two hemichordate nerve cords. Support for both ideas has been claimed from morphology and from evodevo. Thus, at present, the question of the ancestral deuterostome nervous system remains unresolved.

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Nervous systems and scenarios for the invertebrate-to-vertebrate transition

Professor Nicholas Holland, Scripps Research Institute, La Jolla, USA

Abstract

During the past 150 years, scenarios for the evolutionary origin of vertebrates from invertebrates have typically given the nervous system top billing. This neural emphasis began in an era when Homo sapiens was positioned at the summit of an evolutionary tree shaped almost exclusively by progressive evolution, such that human brains were best of all. By now these old viewpoints have changed. Tree thinking has positioned all extant organisms equidistant from the root of the tree, and molecular phylogenies have revealed an unexpected prevalence of regressive evolution. Even so, current theories of vertebrate origin remain neurocentric, in part because the complexity of many nervous systems makes them a rich source of characters for comparative biology at all levels of organisation, and in part because the two currently prominent and contending scenarios of vertebrate origin have their roots, respectively, in the nineteenth century annelid and enteropneust theories that were both strongly focused on the nervous system. At present, not surprisingly, some of the most perplexing questions about the origin of the vertebrates prominently concern the nervous system. For example, is the apical nervous system of many invertebrate larvae a central feature or only a deceptive side issue for big-picture evolution?; and, even more fundamentally, is the nervous system rudimentary or lacking in some phyla because it was never there in the first place or because it was formerly present but suffered regressive evolution? The present review considers scenarios for the invertebrate-to-vertebrate transition with special attention to nervous system evolution.

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Evolution of brains and minds

Professor Gerhard Roth, University of Bremen, Germany

Abstract

Complex brains and complex cognitive abilities have evolved several times within the animal kingdom, e.g., in arthropods/insects (especially social insects like honeybees), molluscs /cephalopods (particularly octopodids), birds (especially corvid birds and parrots) and mammals (especially primates including Homo sapiens). However, contrary to popular views of evolution these cases are relatively rare; the vast majority of animals have simple nervous systems or brains and modest cognitive abilities either because of resting at a “primitive” ancestral state, or by secondary simplification. Even when accepting the presence of an ancestral tripartite brain common to all bilaterians, it appears to be likely that the mentioned cases of complex brains and cognitive abilities have evolved independently. This would, among others, include the much discussed question of homology of “mushroom bodies” in the different groups of arthropods and of the cerebral cortex of mammals and the meso-nidopallium of birds among amniote vertebrates. Besides selective pressures on “ecological” and “social” intelligence, which is of importance to birds and mammals, respectively, the universal dominant selective factor seems to be an increase in general intelligence (or high information processing speed) in the context of new, complex and unpredictable environments.