Immunolocalization of serotonin in Onychophora argues against segmental ganglia being an ancestral feature of arthropods

Springer Science and Business Media LLC - Tập 7 - Trang 1-9 - 2007
Georg Mayer1, Steffen Harzsch2
1Department of Anatomy and Cell Biology, University of Melbourne, Australia
2Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany

Tóm tắt

Onychophora (velvet worms) represent the most basal arthropod group and play a pivotal role in the current discussion on the evolution of nervous systems and segmentation in arthropods. Although there is a wealth of information on the immunolocalization of serotonin (5-hydroxytryptamine, 5-HT) in various euarthropods, as yet no comparable localization data are available for Onychophora. In order to understand how the onychophoran nervous system compares to that of other arthropods, we studied the distribution of serotonin-like immunoreactive neurons and histological characteristics of ventral nerve cords in Metaperipatus blainvillei (Onychophora, Peripatopsidae) and Epiperipatus biolleyi (Onychophora, Peripatidae). We demonstrate that paired leg nerves are the only segmental structures associated with the onychophoran nerve cord. Although the median commissures and peripheral nerves show a repeated pattern, their arrangement is independent from body segments characterized by the position of legs and associated structures. Moreover, the somata of serotonin-like immunoreactive neurons do not show any ordered arrangement in both species studied but are instead scattered throughout the entire length of each nerve cord. We observed neither a serially iterated nor a bilaterally symmetric pattern, which is in contrast to the strictly segmental arrangement of serotonergic neurons in other arthropods. Our histological findings and immunolocalization experiments highlight the medullary organization of the onychophoran nerve cord and argue against segmental ganglia of the typical euarthropodan type being an ancestral feature of Onychophora. These results contradict a priori assumptions of segmental ganglia being an ancestral feature of arthropods and, thus, weaken the traditional Articulata hypothesis, which proposes a sistergroup relationship of Annelida and Arthropoda.

Tài liệu tham khảo

Nielsen C: Animal Evolution: Interrelationships of the Living Phyla. 2001, Oxford: Oxford University Press Kusche K, Ruhberg H, Burmester T: A hemocyanin from the Onychophora and the emergence of respiratory proteins. Proc Natl Acad Sci USA. 2002, 99: 10545-10548. 10.1073/pnas.152241199. Mayer G, Ruhberg H, Bartolomaeus T: When an epithelium ceases to exist – an ultrastructural study on the fate of the embryonic coelom in Epiperipatus biolleyi (Onychophora, Peripatidae). Acta Zool. 2004, 85: 163-170. 10.1111/j.0001-7272.2004.00166.x. Regier JC, Shultz JW, Kambic RE: Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc R Soc B. 2005, 272: 395-401. 10.1098/rspb.2004.2917. Vítková M, Král J, Traut W, Zrzavy J, Marec F: The evolutionary origin of insect telomeric repeats, (TTAGG)n. Chromosome Res. 2005, 13: 145-156. 10.1007/s10577-005-7721-0. Mallatt J, Giribet G: Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phyl Evol. 2006, 40: 772-794. 10.1016/j.ympev.2006.04.021. Monge-Nájera J, Hou X: Experimental taphonomy of velvet worms (Onychophora) and implications for the Cambrian "explosion, disparity and decimation" model. Rev Biol Trop. 2002, 50: 1133-1138. Budd GE: Why are arthropods segmented?. Evol Dev. 2001, 3: 332-342. 10.1046/j.1525-142X.2001.01041.x. Eriksson BJ, Tait NN, Budd GE: Head development in the onychophoran Euperipatoides kanangrensis. With particular reference to the central nervous system. J Morphol. 2003, 255: 1-23. 10.1002/jmor.10034. Mayer G: Origin and differentiation of nephridia in the Onychophora provide no support for the Articulata. Zoomorphology. 2006, 125: 1-12. 10.1007/s00435-005-0006-5. Mayer G: Structure and development of onychophoran eyes – what is the ancestral visual organ in arthropods?. Arthropod Struct Dev. 2006, 35: 231-245. 10.1016/j.asd.2006.06.003. Scholtz G: The Articulata hypothesis – or what is a segment?. Org Divers Evol. 2002, 2: 197-215. 10.1078/1439-6092-00046. Scholtz G: Is the taxon Articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods. The new Panorama of Animal Evolution. Proceedings of the 18th Inernational Congress of Zoology. Edited by: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M. 2003, Sofia: Pensoft, 489-501. Giribet G: Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology. 2003, 106: 303-326. 10.1078/0944-2006-00131. Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR: The position of the Arthropoda in the phylogenetic system. J Morphol. 1998, 238: 263-285. 10.1002/(SICI)1097-4687(199812)238:3<263::AID-JMOR1>3.0.CO;2-L. Scholtz G, Edgecombe GD: The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol. 2006, 216: 395-415. 10.1007/s00427-006-0085-4. Wägele J-W, Erikson T, Lockhart P, Misof B: The Ecdysozoa: artifact or monophylum?. J Zool Syst Evol Res. 1999, 37: 211-223. Ax P: Multicellular Animals. The Phylogenetic System of the Metazoa. 2000, Berlin: Springer Wägele J-W, Misof B: On quality of evidence in phylogeny reconstruction: a reply to Zrzavý's defence of the 'Ecdysozoa' hypothesis. J Zool Syst Evol Res. 2001, 39: 165-176. 10.1046/j.1439-0469.2001.00177.x. Orrhage L, Müller MCM: Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia. 2005, 535/536: 79-111. 10.1007/s10750-004-4375-4. Müller MCM: Polychaete nervous systems: Ground pattern and variations – cLS microscopy and the importance of novel characteristics in phylogenetic analysis. Integr Comp Biol. 2006, 46: 125-133. 10.1093/icb/icj017. Kristensen RM, Higgins RP: Kinorhyncha. Microscopic Anatomy of Invertebrates. Edited by: Harrison FW, Ruppert EE. 1991, New York: Wiley-Liss, 4: 377-404. Sedgwick A: The development of the Cape species of Peripatus. Part III. On the changes from stage A to stage F. Q J Microsc Sci. 1887, 27: 467-550. Fedorow B: Zur Anatomie des Nervensystems von Peripatus. I. Das Neurosomit von Peripatus tholloni. Zool Jb Anat. 1926, 48: 273-310. Schürmann FW: Common and special features of the nervous system of Onychophora: A comparison with Arthropoda, Annelida and some other invertebrates. The Nervous System of Invertebrates: an Evolutionary and Comparative Approach. Edited by: Breidbach O, Kutsch W. 1995, Basel: Birkhäuser, 139-158. Hessling R, Westheide W: Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonelia viridis. J Morphol. 2002, 252: 100-113. 10.1002/jmor.1093. Hessling R: Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia. 2003, 496: 225-239. 10.1023/A:1026153016913. McHugh D: Molecular evidence that echiurans and pogonophorans are derived annelids. Proc Natl Acad Sci USA. 1997, 94: 8006-8009. 10.1073/pnas.94.15.8006. Brown S, Rouse GW, Hutchings P, Colgan D: Assessing the usefulness of histone H3, U2 snRNA and 28S rDNA in analyses of polychaete relationships. Aust J Zool. 1999, 47: 499-516. 10.1071/ZO99026. Bleidorn C, Vogt L, Bartolomaeus T: New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Mol Phyl Evol. 2003, 29: 279-288. 10.1016/S1055-7903(03)00107-6. Jördens J, Struck T, Purschke G: Phylogenetic inference regarding Parergodrilidae and Hrabeiella periglandulata ('Polychaeta', Annelida) based on 18S rDNA, 28S rDNA and COI sequences. J Zool Syst Evol Res. 2004, 42: 270-280. 10.1111/j.1439-0469.2004.00265.x. Colgan DJ, Hutchings PA, Braune M: A multigene framework for polychaete phylogenetic studies. Org Divers Evol. 2006, 6: 220-235. 10.1016/j.ode.2005.11.002. Spörhase-Eichmann U, Gras H, Schürmann F-W: Patterns of serotonin-immunoreactive neurons in the central nervous system of the earthworm Lumbricus terrestris L. I. Ganglia of the ventral nerve cord. Cell Tissue Res. 1987, 1987: 601-614. Harzsch S, Müller CHG, Wolf H: From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister-group relationship of Chelicerata and "Myriapoda" but favour the Mandibulata concept. Dev Genes Evol. 2005, 215: 53-68. 10.1007/s00427-004-0451-z. Harzsch S: Neurophylogeny: Architecture of the nervous system and a fresh view on arthropod phyologeny. Integr Comp Biol. 2006, 46: 162-194. 10.1093/icb/icj011. Harzsch S, Waloszek D: Serotonin-immunoreactive neurons in the ventral nerve cord of Crustacea: a character to study aspects of arthropod phylogeny. Arthropod Struct Dev. 2000, 29: 307-322. 10.1016/S1467-8039(01)00015-9. Harzsch S: Evolution of identified arthropod neurons: the serotonergic system in relation to engrailed-expressing cells in the embryonic ventral nerve cord of the American lobster Homarus americanus Milne Edwards, 1873 (Malacostraca, Pleocyemata, Homarida). Dev Biol. 2003, 258: 44-56. 10.1016/S0012-1606(03)00113-1. Harzsch S: Phylogenetic comparison of serotonin-immunoreactive neurons in representatives of the Chilopoda, Diplopoda, and Chelicerata: implications for arthropod relationships. J Morphol. 2004, 259: 198-213. 10.1002/jmor.10178. Gardner CR, Robson EA: A response to monoamines in Peripatopsis moseleyi (Onychophora). Experientia. 1978, 34: 1576-1577. 10.1007/BF02034682. Gardner CR, Robson EA, Stanford C: The presence of monoamines in the nervous system of Peripatopsis (Onychophora). Experientia. 1978, 34: 1577-1578. 10.1007/BF02034683. Strausfeld NJ, Strausfeld CM, Loesel R, Rowell D, Stowe S: Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc R Soc B. 2006, 273: 1857-1866. 10.1098/rspb.2006.3536. Strausfeld NJ, Strausfeld C, Stowe S, Rowell D, Loesel R: The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli. Arthropod Struct Dev. 2006, 35: 169-196. 10.1016/j.asd.2006.06.002. Schürmann FW, Sandeman DC: Giant fibres in the ventral nerve cord of Peripatoides leuckarti (Onychophora). Naturwissenschaften. 1976, 63: 580-581. 10.1007/BF00622801. Reuter M, Halton DW: Comparative neurobiology of Platyhelminthes. Interrelationships of the platyhelminthes. Edited by: Littlewood D, Bray RA. 2001, London: Taylor and Francis, 239-249. Kotikova EA, Raikova OI, Reuter M, Gustafsson MKS: The nervous and muscular systems in the free-living flatworm Castrella truncata (Rhabdocoela): an immunocytochemical and phalloidin fluorescence study. Tissue Cell. 2002, 34: 365-374. 10.1016/S004081660200037X. Müller MCM, Sterrer W: Musculature and nervous system of Gnathostomula peregrina (Gnathostomulida) shown by phalloidin labeling, immunohistochemistry, and cLSM, and their phylogenetic significance. Zoomorphology. 2004, 123: 169-177. Bullock TH, Horridge GA: Structure and Function in the Nervous Systems of Invertebrates. 1965, San Francisco: Freeman Company Voronezhskaya EE, Tyurin SA, Nezlin LP: Neuronal development in larval chiton Ischnochiton hakodadensis (Mollusca: Polyplacophora). J Comp Neurol. 2002, 444: 25-38. 10.1002/cne.10130. Eriksson BJ, Larson ET, Thörnquist P-O, Tait N, Budd GE: Expression of engrailed in the developing brain and appendages of the onychophoran Euperipatoides kanangrensis (Reid). J Exp Zool (Mol Dev Evol). 2005, 304B: 1-9. 10.1002/jez.b.21030. Scholtz G, Edgecombe GD: Heads, Hox and the phylogenetic position of trilobites. Crustacea and Arthropod Phylogeny. Edited by: Koenemann S, Jenner R, Vonk R. 2005, Boca Raton: CRC Press, 16: 139-165. Fedorow B: Zur Anatomie des Nervensystems von Peripatus. II. Das Nervensystem des vorderen Körperendes und seine Metamerie. Zool Jb Anat. 1929, 50: 279-332. Birket-Smith SJR: The anatomy of the body wall of Onychophora. Zool Jb Anat. 1974, 93: 123-154. Hoyle G, Williams M: The musculature of Peripatus and its innervation. Philos Trans R Soc Lond B. 1980, 288: 481-510. 10.1098/rstb.1980.0024. Storch V, Ruhberg H: Onychophora. Microscopic Anatomy of Invertebrates. Edited by: Harrison FW, Rice ME. 1993, New York: Wiley-Liss, 12: 11-56. von Kennel J: Entwicklungsgeschichte von Peripatus edwardsii Blanch. und Peripatus torquatus n.sp. II. Theil. Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg. 1888, 8: 1-93. Mayer G, Bartolomaeus T, Ruhberg H: Ultrastructure of mesoderm in embryos of Opisthopatus roseus (Onychophora, Peripatopsidae): Revision of the "Long Germ Band" hypothesis for Opisthopatus. J Morphol. 2005, 263: 60-70. 10.1002/jmor.10289. Whitington PM: The evolution of arthropod nervous systems: Insights from neural development in the Onychophora and Myriapoda. Theories, Development, Invertebrates. From Series Evolution of Nervous Systems. Edited by: Striedler GF, Rubenstein JLR, Kaas JH. 2006, Oxford: Academic Press, 317-336. Heidenhain M: Über die Mallory'sche Bindegewebsfärbung mit Karmin und Azokarmin als Vorfarben. Z wiss Mikrosk. 1915, 33: 361-372. Beltz BS, Kravitz EA: Mapping of serotonin-like immunoreactivity in the lobster nervous system. J Neurosci. 1983, 3: 585-602.