An Option Space for Early Neural Evolution

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 emphasize the role of nervous systems in coordinating multicellular activity, especially muscle-based motility. Here we consider both frameworks and apply them to describe aspects of each of three main groups of phenomena that nervous systems control: behavior, 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 an overview of the many influences and constraints that may have played a role in the evolution of the first nervous systems.

[1]  S. Leys,et al.  The hidden biology of sponges and ctenophores. , 2015, Trends in ecology & evolution.

[2]  D. Prober,et al.  Melatonin Is Required for the Circadian Regulation of Sleep , 2015, Neuron.

[3]  F. Keijzer Moving and sensing without input and output: early nervous systems and the origins of the animal sensorimotor organization , 2015, Biology & Philosophy.

[4]  L. Moroz Convergent evolution of neural systems in ctenophores , 2015, Journal of Experimental Biology.

[5]  M. Nikitin Bioinformatic prediction of Trichoplax adhaerens regulatory peptides. , 2015, General and comparative endocrinology.

[6]  Wolfgang Petrich,et al.  A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge , 2015, BMC Biology.

[7]  G. Jékely,et al.  The phylogenetic position of ctenophores and the origin(s) of nervous systems , 2015, EvoDevo.

[8]  Y. Jan,et al.  Identification of motor neurons and a mechanosensitive sensory neuron in the defecation circuitry of Drosophila larvae , 2014, eLife.

[9]  S. Eaton,et al.  Delivery of circulating lipoproteins to specific neurons in the Drosophila brain regulates systemic insulin signaling , 2014, eLife.

[10]  D. Bucher,et al.  Melatonin Signaling Controls Circadian Swimming Behavior in Marine Zooplankton , 2014, Cell.

[11]  Jeffrey S. Guasto,et al.  Vortical ciliary flows actively enhance mass transport in reef corals , 2014, Proceedings of the National Academy of Sciences.

[12]  D. Arendt,et al.  Evolution: Ctenophore Genomes and the Origin of Neurons , 2014, Current Biology.

[13]  M. Martindale,et al.  Developmental and light-entrained expression of melatonin and its relationship to the circadian clock in the sea anemone Nematostella vectensis , 2014, EvoDevo.

[14]  J. Ryan Did the ctenophore nervous system evolve independently? , 2014, Zoology.

[15]  R. Reiter,et al.  A review of the melatonin functions in zebrafish physiology , 2014, Journal of pineal research.

[16]  Victor V. Solovyev,et al.  The Ctenophore Genome and the Evolutionary Origins of Neural Systems , 2014, Nature.

[17]  G. Jensen,et al.  Marine Tubeworm Metamorphosis Induced by Arrays of Bacterial Phage Tail–Like Structures , 2014, Science.

[18]  Nicholas H. Putnam,et al.  The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution , 2013, Science.

[19]  C. Nielsen Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea? , 2013, BMC Evolutionary Biology.

[20]  Olivier Meste,et al.  Melanin-concentrating hormone regulates beat frequency of ependymal cilia and ventricular volume , 2013, Nature Neuroscience.

[21]  L. Schoofs,et al.  Neuropeptides control life-phase transitions , 2013, Proceedings of the National Academy of Sciences.

[22]  S. Tunaru,et al.  Conserved MIP receptor–ligand pair regulates Platynereis larval settlement , 2013, Proceedings of the National Academy of Sciences.

[23]  Fred Keijzer,et al.  What nervous systems do: early evolution, input–output, and the skin brain thesis , 2013, Adapt. Behav..

[24]  Toshio Takahashi,et al.  Neuropeptides trigger oocyte maturation and subsequent spawning in the hydrozoan jellyfish Cytaeis uchidae , 2013, Molecular reproduction and development.

[25]  Raymond E Goldstein,et al.  Hydrodynamic synchronization and metachronal waves on the surface of the colonial alga Volvox carteri. , 2012, Physical review letters.

[26]  E. Houliston,et al.  A conserved function for Strabismus in establishing planar cell polarity in the ciliated ectoderm during cnidarian larval development , 2012, Development.

[27]  N. Webster,et al.  Crustose Coralline Algae and a Cnidarian Neuropeptide Trigger Larval Settlement in Two Coral Reef Sponges , 2012, PloS one.

[28]  S. Özbek,et al.  Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones , 2012, Proceedings of the Royal Society B: Biological Sciences.

[29]  Todd H. Oakley,et al.  Cnidocyte discharge is regulated by light and opsin-mediated phototransduction , 2012, BMC Biology.

[30]  T. Münch,et al.  Neuropeptides regulate swimming depth of Platynereis larvae , 2011, Proceedings of the National Academy of Sciences.

[31]  C. Borchiellini,et al.  Dissecting the PCP pathway: One or more pathways? , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[32]  H. Reichert,et al.  Complex neural architecture in the diploblastic larva of Clava multicornis (Hydrozoa, Cnidaria) , 2011, The Journal of comparative neurology.

[33]  F. Raible,et al.  Another place, another timer: Marine species and the rhythms of life , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[34]  G. Jékely Origin and early evolution of neural circuits for the control of ciliary locomotion , 2011, Proceedings of the Royal Society B: Biological Sciences.

[35]  T. Sutherland,et al.  Harnessing disorder: onychophorans use highly unstructured proteins, not silks, for prey capture , 2010, Proceedings of the Royal Society B: Biological Sciences.

[36]  K. Sawamoto,et al.  Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia , 2010, Nature Cell Biology.

[37]  B. Degnan,et al.  The initiation of metamorphosis as an ancient polyphenic trait and its role in metazoan life-cycle evolution , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[38]  S. Degnan,et al.  Carry‐over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina , 2009, Molecular ecology.

[39]  A. Ereskovsky,et al.  Origin of the neuro-sensory system: new and expected insights from sponges. , 2009, Integrative zoology.

[40]  Yehuda Ben-Shahar,et al.  Motile Cilia of Human Airway Epithelia Are Chemosensory , 2009, Science.

[41]  G. Miller Origins. On the origin of the nervous system. , 2009, Science.

[42]  Clare C. Yu,et al.  The PCP Pathway Instructs the Planar Orientation of Ciliated Cells in the Xenopus Larval Skin , 2009, Current Biology.

[43]  Corinne Da Silva,et al.  Phylogenomics Revives Traditional Views on Deep Animal Relationships , 2009, Current Biology.

[44]  H. Hausen,et al.  Mechanism of phototaxis in marine zooplankton , 2008, Nature.

[45]  Romain Derelle,et al.  A maternally localised Wnt ligand required for axial patterning in the cnidarian Clytia hemisphaerica , 2008, Development.

[46]  A. Maule,et al.  Effects of neuropeptide F on regeneration in Girardia tigrina (Platyhelminthes) , 2008, Cell and Tissue Research.

[47]  S. Leys,et al.  Coordinated contractions effectively expel water from the aquiferous system of a freshwater sponge , 2007, Journal of Experimental Biology.

[48]  B. Degnan,et al.  Wnt and TGF-β Expression in the Sponge Amphimedon queenslandica and the Origin of Metazoan Embryonic Patterning , 2007, PloS one.

[49]  Boris Guirao,et al.  Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia. , 2007, Biophysical journal.

[50]  L. Moroz,et al.  Signaling mechanisms underlying metamorphic transitions in animals. , 2006, Integrative and comparative biology.

[51]  M. Adams,et al.  A Command Chemical Triggers an Innate Behavior by Sequential Activation of Multiple Peptidergic Ensembles , 2006, Current Biology.

[52]  C. Nielsen Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. , 2005, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[53]  E. Hafen,et al.  Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Ma,et al.  Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[55]  S. Tyler,et al.  Adhesive organs of the gastrotricha , 1980, Zoomorphologie.

[56]  L. Melanson,et al.  Adhesive organs of the gastrotricha , 1980, Zoomorphologie.

[57]  G. Martin Ciliary gliding in lower invertebrates , 1978, Zoomorphologie.

[58]  G. Martin A new function of rhabdites: Mucus production for ciliary gliding , 1978, Zoomorphologie.

[59]  E. Ziegelmeier Neue Untersuchungen über die Wohnröhren-Bauweise vonLanice conchilega (Polychaeta, Sedentaria) , 1969, Helgoländer wissenschaftliche Meeresuntersuchungen.

[60]  A. Tarrant,et al.  Endocrine-like Signaling in Cnidarians: Current Understanding and Implications for Ecophysiology1 , 2005, Integrative and comparative biology.

[61]  Michael Nickel,et al.  Kinetics and rhythm of body contractions in the sponge Tethya wilhelma (Porifera: Demospongiae) , 2004, Journal of Experimental Biology.

[62]  G. Mackie Central Neural Circuitry in the Jellyfish Aglantha , 2004, Neurosignals.

[63]  C. Nielsen Trochophora larvae: cell-lineages, ciliary bands, and body regions. 1. Annelida and Mollusca. , 2004, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[64]  M. Anctil Ultrastructure of the luminescent system of the ctenophore Mnemiopsis leidyi , 1985, Cell and Tissue Research.

[65]  G. Martin The duo-gland adhesive system of the archiannelidsProtodrilus andSaccocirrus and the turbellarianMonocelis , 1978, Zoomorphologie.

[66]  J. A. Westfall The nematocyte complex in a hydromedusan, Gonionemus vertens , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[67]  M. Maldonado,et al.  The cellular basis of photobehavior in the tufted parenchymella larva of demosponges , 2003 .

[68]  S. Kuang,et al.  Serotonergic sensory-motor neurons mediate a behavioral response to hypoxia in pond snail embryos. , 2002, Journal of neurobiology.

[69]  R. Nusse,et al.  Ablation of Insulin-Producing Neurons in Flies: Growth and Diabetic Phenotypes , 2002, Science.

[70]  T. Lacalli,et al.  Locomotory and feeding effectors of the tornaria larva of Balanoglossus biminiensis , 2002 .

[71]  B. Degnan,et al.  Cytological Basis of Photoresponsive Behavior in a Sponge Larva , 2001, The Biological Bulletin.

[72]  A. Noë,et al.  A sensorimotor account of vision and visual consciousness. , 2001, The Behavioral and brain sciences.

[73]  J. Khattra,et al.  Recent Advances in Our Knowledge of the Myxozoa , 2001, The Journal of eukaryotic microbiology.

[74]  E. Hafen,et al.  An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control , 2001, Current Biology.

[75]  V. Paul,et al.  Natural Chemical Cues for Settlement and Metamorphosis of Marine-Invertebrate Larvae , 2001 .

[76]  M. Hadfield,et al.  The apical sensory organ of a gastropod veliger is a receptor for settlement cues. , 2000, The Biological bulletin.

[77]  T. Ueda,et al.  Dynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence. , 1999, Bio Systems.

[78]  S. Tyler,et al.  Functional morphology of musculature in the acoelomate worm, Convoluta pulchra (Plathelminthes) , 1999, Zoomorphology.

[79]  R. Meech,et al.  Impulse conduction in a sponge. , 1999, The Journal of experimental biology.

[80]  Stokes Larval locomotion of the lancelet , 1997, The Journal of experimental biology.

[81]  G. Mackie The Elementary Nervous System Revisited , 1990 .

[82]  C. Hunter,et al.  Reproduction and recruitment of corals : comparisons among the Caribbean, the Tropical Pacific, and the Red Sea , 1990 .

[83]  C. Jarvis,et al.  Correlated electrophysiology and morphology of the ependyma in rat hypothalamus , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  C. Lent,et al.  Excitability and secretory activity in the salivary gland cells of jawed leeches (Hirudinea: Gnathobdellida). , 1988, The Journal of experimental biology.

[85]  L. Buss LIFE CYCLE EVOLUTION , 1988 .

[86]  A. Moss,et al.  Unilateral ciliary reversal and motor responses during prey capture by the ctenophore Pleurobrachia. , 1985, The Journal of experimental biology.

[87]  S. Tamm Mechanical synchronization of ciliary beating within comb plates of ctenophores. , 1984, The Journal of experimental biology.

[88]  V. Braitenberg Vehicles, Experiments in Synthetic Psychology , 1984 .

[89]  K. Bailey,et al.  A laboratory study of predation by Aurelia aurita on larval herring (Clupea harengus): Experimental observations compared with model predictions , 1983 .

[90]  R. A. Cloney Ascidian Larvae and the Events of Metamorphosis , 1982 .

[91]  J. Franc ORGANIZATION AND FUNCTION OF CTENOPHORE COLLOBLASTS: AN ULTRASTRUCTURAL STUDY , 1978 .

[92]  T. Yamamoto,et al.  Studies on neural mechanisms of the gustatory‐salivary reflex in rabbits. , 1978, The Journal of physiology.

[93]  S. B. Kater,et al.  Physiological and morphological evidence for coupling in mouse salivary gland acinar cells , 1978, The Journal of cell biology.

[94]  S. Kater,et al.  Propagation of action potentials through electrotonic junctions in the salivary glands of the pulmonate mollusc, Helisoma trivolvis. , 1978, The Journal of experimental biology.

[95]  W. E. Schwab The ontogeny of swimming behavior in the scyphozoan, Aurelia aurita. I. Electrophysiological analysis. , 1977, The Biological bulletin.

[96]  E. R. Trueman,et al.  The locomotion of soft-bodied animals , 1975 .

[97]  M. P. de Ceccatty The Origin of the Integrative Systems: A Change in View Derived from Research on Coelenterates and Sponges , 2015, Perspectives in biology and medicine.

[98]  M. P. Ceccatty The origin of the integrative systems: a change in view derived from research on coelenterates and sponges. , 1974 .

[99]  M. Hernandez-Nicaise Ultrastructural evidence for a sensory-motor neuron in Ctenophora. , 1974, Tissue & cell.

[100]  G. Mackie Neuroid Conduction and the Evolution of Conducting Tissues , 1970, The Quarterly Review of Biology.

[101]  G. Horridge,et al.  Primitive Nervous Systems , 1968, Nature.

[102]  L. Passano PACEMAKERS AND ACTIVITY PATTERNS IN MEDUSAE: HOMAGE TO ROMANES. , 1965, American zoologist.

[103]  D. A. Dorsett,et al.  The behaviour of polydora ciliata (Johnst.). Tube-building and burrowing , 1961, Journal of the Marine Biological Association of the United Kingdom.

[104]  J. Chang Analysis of the luminescent response of the ctenophore, Mnemiopsis leidyi, to stimulation. , 1954, Journal of cellular and comparative physiology.

[105]  G. Parker THE ELEMENTARY NERVOUS SYSTEM , 1919 .

[106]  W. Smith The Integrative Action of the Nervous System , 1907, Nature.

[107]  Origin of the Nervous System , 1881, The Dental register.