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Abstract

The current view of early metazoan phylogeny suggests that the bilaterian body plan arose only once during evolution. This first urbilaterian animal was most likely equipped with an anterior condensation of nerve cells – a brain – from which all brains of modern animals have diverged. Until recently, the ancestor of all bilaterian phyla was viewed as a very simple animal with an accordingly simple brain. Molecular studies, however, demonstrate a multitude of homologous genes that are expressed in similar patterns in the developing brains of vertebrates, insects, and annelids. Taken together, these findings imply that the anatomy of the urbilaterian cerebrum might have been more elaborate than previously assumed. If true, ancient architectural features might have been conserved during evolution and should be identifiable in distantly related modern animal phyla. Comparative studies on representatives of arthropods, onychophorans, and annelids suggest that this is indeed the case. This chapter summarizes recent neuroanatomical surveys that aim to retrace the early evolution of the metazoan brain and to use neuroanatomical data to test conflicting hypothesis on phylogenetic relationships between major animal phyla.

This chapter is based on the habilitation thesis of R.Loesel

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References

  • Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Åkesson B (1963) The comparative morphology and embryology of the head in scale worms (Aphroditidae, Polychaeta). Ark Zool 16:125–163

    Google Scholar 

  • Bartolomaeus T, Purschke G, Hausen H (2005) Polychaete phylogeny based on morphological data – a comparison of current attempts. Hydrobiologia 535(536):341–356

    Article  Google Scholar 

  • Bodian D (1937) A new method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat Rec 69:153–162

    Article  CAS  Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous system of invertebrates. Freeman, San Francisco

    Google Scholar 

  • Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy. Evolution and adaption. Wiley, New York

    Book  Google Scholar 

  • Cajal SR (1911) Histologie du système nerveux de l’Homme et des vertébrés. Maloine, Paris. This is the French translation of Cajal’s original textura del sistema nervioso del Hombre y los vertebrados from 1894

    Google Scholar 

  • Chase R, Tolloczko B (1993) Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Micrsc Res Tech 24:214–230

    Article  CAS  Google Scholar 

  • Clarke DD, Sokoloff L (1999) Circulation and energy metabolism of the brain. In: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD (eds) Basic neurochemistry: molecular. Cellular and medical aspects. Lippincott-Raven, Philadelphia, pp 637–669

    Google Scholar 

  • Cuvier G (1817) Le règne animal, vol II. Déterville, Paris

    Google Scholar 

  • Dohle W (2001) Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name ‘Tetraconata’ for the monophyletic unit Crustacea + Hexapoda. In: Deuve T (ed) Origin of the hexapoda. Ann Soc Entomol Fr 37:85–103

    Google Scholar 

  • Dorsett DA, Hyde R (1969) The fine structure of the compound sense organs on the cirri of Nereis diversicolor. Z Zellforsch 97:512–527

    Article  PubMed  CAS  Google Scholar 

  • Eernisse DJ (1997) Arthropod and annelid relationships reexamined. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman and Hall, London, pp 43–56

    Google Scholar 

  • Egelhaaf M, Borst A (1993) Motion computation and visual orientation in flies. Comp Biochem Physiol 104A:659–673

    Article  Google Scholar 

  • Eisthen HL (2002) Why are olfactory systems of different animals so similar? Brain Behav Evol 59:273–293

    Article  PubMed  Google Scholar 

  • Farris SM (2005) Evolution of insect mushroom bodies: old clues, new insights. Arthropod Struct Dev 34:211–234

    Article  Google Scholar 

  • Farris SM, Roberts NS (2005) Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects. Proc Natl Acad Sci USA 102:17394–17399

    Article  PubMed  CAS  Google Scholar 

  • Golgi C (1873) Sulla struttura della sostanza grigia del cervello. Gazz Med Ital Lomb 33:244–246

    Google Scholar 

  • Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 436:474–489

    Article  Google Scholar 

  • Hanesch U, Fischbach KF, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257:343–366

    Article  Google Scholar 

  • Hanström B (1928) Vergleichende anatomie des nervensystems der wirbellosen tiere unter berücksichtigung seiner funktion. Springer, Berlin

    Google Scholar 

  • Harzsch S (2002) Neurobiologie und evolutionsforschung: “Neurophylogenie” und die stammesgeschichte der euarthropoda. Neuroforum 4(02):267–273

    Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4(4):266–275

    Article  PubMed  CAS  Google Scholar 

  • Hennig W (1950) Grundzüge einer theorie der phylogenetischen systematik. Deutscher Zentralverlag, Berlin

    Google Scholar 

  • Heuer CM, Loesel R (2008) Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida). Cell Tissue Res 331:713–724

    Article  PubMed  CAS  Google Scholar 

  • Heuer CM, Loesel R (2009) Three-dimensional reconstruction of mushroom body neuropils in the polychaete species Nereis diversicolor and Harmothoe areolata (Phyllodocida, Annelida). Zoomorphology 128:219–226

    Article  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: convergent evidence for common principles across phyla. Annu Rev Neurosci 20:595–611

    Article  PubMed  CAS  Google Scholar 

  • Holland ND (2003) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Nat Rev Neurosci 4:617–627

    Article  PubMed  CAS  Google Scholar 

  • Holmgren N (1916) Zur vergleichenden anatomie des gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. K Sven Vetensk Akad Handl 56:1–303

    Google Scholar 

  • Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifera, L.). J Insect Physiol 31:251–264

    Article  Google Scholar 

  • Homberg U (1987) Structure and functions of the central complex in insects. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. Wiley, New York, pp 347–367

    Google Scholar 

  • Homberg U (2004) In search of the sky compass in the insect brain. Naturwissenschaften 91:199–208

    Article  PubMed  CAS  Google Scholar 

  • Homberg U, Reischig T, Stengl M (2003) Neural organization of the circadian system of the cockroach Leucophaea maderae. Chronobiol Int 20(4):577–591

    Article  PubMed  CAS  Google Scholar 

  • Hopkin SP, Read HJ (1992) The biology of millipedes. Oxford University Press, New York

    Google Scholar 

  • Howard J, Blakeslee B, Laughlin SB (1987) The intracellular pupil mechanism and photoreceptor signal – noise ratios in the fly Lucilia-cuprina. Proc R Soc Lond B 231:415–435

    Article  PubMed  CAS  Google Scholar 

  • Ilius M, Wolf R, Heisenberg M (2007) The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open. J Neurogenet 21(4):321–338

    Article  PubMed  CAS  Google Scholar 

  • Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165:427–453

    Article  PubMed  CAS  Google Scholar 

  • Kanzaki R, Arbas EA, Hildebrand JG (1991) Physiology and morphology of protocerebral olfactory neurons in the male moth Manduca sexta. J Comp Physiol A 168:281–298

    Article  PubMed  CAS  Google Scholar 

  • Kutsch W, Breidbach O (1994) Homologous structures in the nervous system of Arthropoda. Adv Insect Physiol 24:1–113

    Article  Google Scholar 

  • Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11(4):475–480

    Article  PubMed  CAS  Google Scholar 

  • Laughlin SB, de van Ruyter Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41

    Article  PubMed  CAS  Google Scholar 

  • Lichtneckert R, Reichert H (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94:465–477

    Article  PubMed  CAS  Google Scholar 

  • Loesel R (2004) Comparative morphology of central neuropils in the brain of arthropods and its evolutionary and functional implications. Acta Biol Hung 55:39–51

    Article  PubMed  CAS  Google Scholar 

  • Loesel R (2006) Can brain structures help to resolve interordinal relationships in insects? Arthropod Syst Phylogeny 64(2):101–106

    Google Scholar 

  • Loesel R, Homberg U (1998) Sustained oscillations in an insect visual system. Naturwissenschaften 85:238–240

    Article  CAS  Google Scholar 

  • Loesel R, Homberg U (1999) Histamine-immunoreactive neurons in the brain of the cockroach Leucophaea maderae. Brain Res 842:408–418

    Article  PubMed  CAS  Google Scholar 

  • Loesel R, Homberg U (2001) Anatomy and physiology of neurons with processes in the accessory medulla of the cockroach, Leucophaea maderae. J Comp Neurol 439(2):193–207

    Article  PubMed  CAS  Google Scholar 

  • Loesel R, Nässel DR, Strausfeld NJ (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31:77–91

    Article  PubMed  Google Scholar 

  • Lowe CJ, Wu M, Salic A, Evans L, Lander E, Stange-Thomann N, Gruber CE, Gerhart J, Kirschner M (2003) Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113:853–865

    Article  PubMed  CAS  Google Scholar 

  • Mallat JM, Garey JR, Schultz JW (2004) Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol 31:178–191

    Article  Google Scholar 

  • McKinzie ME, Benton JL, Beltz BS, Mellon D (2003) Parasol cells of the hemiellipsoid body in the crayfish Procambarus clarkii: dendritic branching patterns and functional implications. J Comp Neurol 462:168–179

    Article  PubMed  Google Scholar 

  • Mori K, Nagao H, Yoshihara Y (1999) The olfactory bulb: coding and processing of odor molecule information. Science 286:711–715

    Article  PubMed  CAS  Google Scholar 

  • Müller CHG, Rosenberg J, Richter S, Meyer-Rochow VB (2003) The compound eye of Scutigera coleoptrata (Linnaeus, 1758) (Chilopoda: Notostigmophora): an ultrastructural reinvestigation that adds support to the Mandibulata concept. Zoomorphology 122:191–209

    Article  Google Scholar 

  • Nässel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326(1):1–24

    Article  PubMed  Google Scholar 

  • Nielsen C (2001) Animal evolution, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Nilsson GE (1996) Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain. J Exp Biol 199:603–607

    PubMed  Google Scholar 

  • Okada R, Rybak J, Manz G, Menzel R (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J Neurosci 27(43):11736–11747

    Article  PubMed  CAS  Google Scholar 

  • Renn SC, Armstrong JD, Yang M, Wang Z, An K, Kaiser K, Taghert PH (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 41:189–207

    Article  PubMed  CAS  Google Scholar 

  • Rössler W, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP (1999) Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 22:9865–9877

    Google Scholar 

  • Roth G, Wullimann MF (1996) Evolution der nervensysteme und sinnesorgane. In: Dudel J, Menzel R, Schmidt RF (eds) Neurowissenschaften. Springer, Berlin, pp 1–31

    Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34(3):257–299

    Article  Google Scholar 

  • Schmucker M, Schneider G (2007) Processing and classification of chemical data inspired by insect olfaction. Proc Natl Acad Sci USA 104(51):20285–20289

    Article  Google Scholar 

  • Scholtz G (2002) The Articulata hypothesis – or what is a segment? Org Divers Evol 2:197–215

    Article  Google Scholar 

  • Scholtz G (2003) Is the taxon articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The new panorama of animal evolution. Proceedings of the 18th international congress of zoology, Pensoft, Sofia, pp 489–501

    Google Scholar 

  • Shear WA (1998) The fossil record and evolution of the Myriapoda. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Systematics association, special vol series 55. Chapman and Hall, London, pp 211–219

    Google Scholar 

  • Sierwald P, Bond JE (2007) Current status of the Myriapod class Diplopoda (Millipedes): taxonomic diversity and phylogeny. Annu Rev Entomol 52:401–410

    Article  PubMed  CAS  Google Scholar 

  • Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ (2003) Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467:150–172

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Heidelberg

    Book  Google Scholar 

  • Strausfeld NJ (1998) Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186–202

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (1999) A brain region in insects that supervises walking. Prog Brain Res 123:273–284

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34(3):235–256

    Article  Google Scholar 

  • Strausfeld NJ, Barth FG (1993) Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei. J Comp Neurol 328:43–62

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Hildebrand JG (1999) Olfactory systems: common design, uncommon origins? Curr Opin Neurobiol 9:634–639

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Weltzien P, Barth FG (1993) Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. J Comp Neurol 328:63–75

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Buschbeck EK, Gomez RS (1995) The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser, Basel, pp 349–381

    Chapter  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretation of arthropod mushroom bodies. Learn Mem 5:11–37

    PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Strausfeld CM, Loesel R, Rowell D, Stowe S (2006a) Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc R Soc B 273:1857–1866

    Article  PubMed  Google Scholar 

  • Strausfeld NJ, Strausfeld CM, Stowe S, Rowell D, Loesel R (2006b) The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli. Arthropod Struct Dev 35(3):169–196

    Article  PubMed  CAS  Google Scholar 

  • Strauss R (2003) Control of Drosophila walking and orientation behavior by functional subunits localized in different neuropils in the central brain. In: N Elsner, H Zimmermann (eds) Proceedings of the 29th göttingen neurobiol conference, Thieme, 2003, p 206

    Google Scholar 

  • Struck TH, Schult N, Kusen T, Hickman E, Bleidorn C, McHugh D, Halanych KM (2007) Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol 7:57

    Article  PubMed  Google Scholar 

  • Urbach R, Technau GM (2003) Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Struct Dev 32(1):103–123

    Article  PubMed  Google Scholar 

  • Utting M, Agricola HJ, Sandeman R, Sandeman D (2000) Central complex in the brain of crayfish and its possible homology with that of insects. J Comp Neurol 416:245–261

    Article  PubMed  CAS  Google Scholar 

  • Wägele JW, Misof B (2001) On quality of evidence in phylogeny reconstruction: a reply to Zrzavy’s defence of the ‘Ecdysozoa’ hypothesis. J Zool Syst Evol Res 39:165–176

    Article  Google Scholar 

  • Wägele JW, Erikson T, Lockhart P, Misof B (1999) The Ecdysozoa: artifact or monophylum? J Zool Syst Evol Res 37:211–223

    Article  Google Scholar 

  • Wegerhoff R, Breidbach O, Lobemeier M (1996) Development of locustatachykinin immunopositive neurons in the central complex of the beetle Tenebrio molitor. J Comp Neurol 375:157–166

    Article  PubMed  CAS  Google Scholar 

  • Wheeler WC, Giribet G, Edgecombe GD (2004) Arthropod systematics: the comparative study of genomic, anatomical, and paleontological information. In: Cracraft J, Donoghue MJ (eds) Assembling the tree of life. Oxford University Press, New York, pp 281–318

    Google Scholar 

  • Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool 176:67–86

    Article  Google Scholar 

  • Wollesen T, Loesel R, Wanninger A (2008) Distribution of FMRFamidergic neurons in the central nervous system of the cephalopod mollusc Idiosepius notoides. Acta Biol Hung 59:111–116

    Article  PubMed  Google Scholar 

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Loesel, R. (2011). Neurophylogeny: Retracing Early Metazoan Brain Evolution. In: Pontarotti, P. (eds) Evolutionary Biology – Concepts, Biodiversity, Macroevolution and Genome Evolution. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20763-1_11

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