Journal of Comparative Physiology A

, Volume 203, Issue 8, pp 565–590 | Cite as

The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

  • Christine Martin
  • Vladimir Gross
  • Lars Hering
  • Benjamin Tepper
  • Henry Jahn
  • Ivo de Sena Oliveira
  • Paul Anthony Stevenson
  • Georg MayerEmail author


Understanding the origin and evolution of arthropods requires examining their closest outgroups, the tardigrades (water bears) and onychophorans (velvet worms). Despite the rise of molecular techniques, the phylogenetic positions of tardigrades and onychophorans in the panarthropod tree (onychophorans + tardigrades + arthropods) remain unresolved. Hence, these methods alone are currently insufficient for clarifying the panarthropod topology. Therefore, the evolution of different morphological traits, such as one of the most intriguing features of panarthropods—their nervous system—becomes essential for shedding light on the origin and evolution of arthropods and their relatives within the Panarthropoda. In this review, we summarise current knowledge of the evolution of panarthropod nervous and visual systems. In particular, we focus on the evolution of segmental ganglia, the segmental identity of brain regions, and the visual system from morphological and developmental perspectives. In so doing, we address some of the many controversies surrounding these topics, such as the homology of the onychophoran eyes to those of arthropods as well as the segmentation of the tardigrade brain. Finally, we attempt to reconstruct the most likely state of these systems in the last common ancestors of arthropods and panarthropods based on what is currently known about tardigrades and onychophorans.


Brain Eye Nervous system Velvet worms Water bears 



We are thankful to Noel N. Tait for his assistance with the permits and to Dave M. Rowell, Paul Sunnucks, Noel N. Tait, Franziska A. Franke, Sandra Treffkorn and Michael Gerth for helping to collect the specimens. We also thank Nicole Naumann for assistance with immunohistochemistry, Jörg U. Hammel for his help with SRµCT and all members of the Mayer laboratory for helping with animal husbandry. We gratefully acknowledge Bert R. E. Klagges for providing the anti-synapsin serum. Two anonymous reviewers provided constructive comments, which helped to improve the manuscript. This study was supported by a German Academic Exchange Service (DAAD) scholarship to VG; a Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Brazil: 290029/2010-4) Grant to ISO; a Helmholtz Research Centre Grant (DESY: I-20150213) and the Emmy Noether Programme Funding (Ma 4147/3-1), and an additional Grant (Ma 4147/8-1) of the German Research Foundation (DFG) to GM.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Allwood J, Gleeson D, Mayer G, Daniels S, Beggs JR, Buckley TR (2010) Support for vicariant origins of the New Zealand Onychophora. J Biogeogr 37:669–681CrossRefGoogle Scholar
  2. Arakawa K (2016) No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci USA 113:E3057PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arendt D (2003) Evolution of eyes and photoreceptor cell types. Int J Dev Biol 47:563–571PubMedGoogle Scholar
  4. Arendt D, Wittbrodt J (2001) Reconstructing the eyes of Urbilateria. Philos Trans R Soc B Biol Sci 356:1545–1563CrossRefGoogle Scholar
  5. Arendt D, Hausen H, Purschke G (2009) The ‘division of labour’ model of eye evolution. Philos Trans R Soc B Biol Sci 364:2809–2817CrossRefGoogle Scholar
  6. Baer A, Mayer G (2012) Comparative anatomy of slime glands in Onychophora (velvet worms). J Morphol 273:1079–1088PubMedCrossRefGoogle Scholar
  7. Balfour FM (1883) The anatomy and development of Peripatus capensis. Q J Microsc Sci 23:213–259Google Scholar
  8. Basse A (1906) Beiträge zur Kenntnis des Baues der Tardigraden. Z Wiss Zool 80:259–281Google Scholar
  9. Battelle B-A, Kempler KE, Saraf SR, Marten CE, Dugger DR, Speiser DI, Oakley TH (2015) Opsins in Limulus eyes: characterization of three visible light-sensitive opsins unique to and co-expressed in median eye photoreceptors and a peropsin/RGR that is expressed in all eyes. J Exp Biol 218:466–479PubMedPubMedCentralCrossRefGoogle Scholar
  10. Beckmann H, Hering L, Henze MJ, Kelber A, Stevenson PA, Mayer G (2015) Spectral sensitivity in Onychophora (velvet worms) revealed by electroretinograms, phototactic behaviour and opsin gene expression. J Exp Biol 218:915–922PubMedCrossRefGoogle Scholar
  11. Bemm F, Weiß CL, Schultz J, Förster F (2016) Genome of a tardigrade: horizontal gene transfer or bacterial contamination? Proc Natl Acad Sci USA 113:E3054–E3056PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bitsch C, Bitsch J (2005) Evolution of eye structure and arthropod phylogeny. In: Koenemann S (ed) Crustacea and arthropod relationships. CRC Press, Taylor & Francis Book Inc., New York, pp 81–111Google Scholar
  13. Bitsch J, Bitsch C (2010) The tritocerebrum and the clypeolabrum in mandibulate arthropods: segmental interpretations. Acta Zool 91:249–266CrossRefGoogle Scholar
  14. Boothby TC, Tenlen JR, Smith FW, Wang JR, Patanella KA, Nishimura EO, Tintori SC, Li Q, Jones CD, Yandell M (2015) Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci USA 112:15976–15981PubMedCrossRefGoogle Scholar
  15. Borner J, Rehm P, Schill RO, Ebersberger I, Burmester T (2014) A transcriptome approach to ecdysozoan phylogeny. Mol Phylogenet Evol 80:79–87PubMedCrossRefGoogle Scholar
  16. Boyan GS, Williams JLD, Posser S, Bräunig P (2002) Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthropod Struct Dev 31:65–76PubMedCrossRefGoogle Scholar
  17. Boyan GS, Bräunig P, Posser S, Williams JLD (2003) Embryonic development of the sensory innervation of the clypeo–labral complex: further support for serially homologous appendages in the locust. Arthropod Struct Dev 32:289–302PubMedCrossRefGoogle Scholar
  18. Brenneis G (2016) Pycnogonida. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 419–427Google Scholar
  19. Brenneis G, Richter S (2010) Architecture of the nervous system in Mystacocarida (Arthropoda, Crustacea)—an immunohistochemical study and 3D reconstruction. J Morphol 271:169–189PubMedGoogle Scholar
  20. Brenneis G, Scholtz G (2014) The ‘ventral organs’ of Pycnogonida (Arthropoda) are neurogenic niches of late embryonic and post-embryonic nervous system development. PLoS One 9:e95435PubMedPubMedCentralCrossRefGoogle Scholar
  21. Brenneis G, Scholtz G (2015) Serotonin-immunoreactivity in the ventral nerve cord of Pycnogonida—support for individually identifiable neurons as ancestral feature of the arthropod nervous system. BMC Evol Biol 15:136PubMedPubMedCentralCrossRefGoogle Scholar
  22. Brenneis G, Ungerer P, Scholtz G (2008) The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment. Evol Dev 10:717–724PubMedCrossRefGoogle Scholar
  23. Brinck P (1957) Onychophora, a review of South African species, with a discussion on the significance of the geographical distribution of the group. In: Hanström B, Brinck P, Rudebeck G (eds) South African animal life. Almqvist & Wiksell, Stockholm, pp 7–32Google Scholar
  24. Briscoe AD (2000) Six opsins from the butterfly Papilio glaucus: molecular phylogenetic evidence for paralogous origins of red-sensitive visual pigments in insects. J Mol Evol 51:110–121PubMedCrossRefGoogle Scholar
  25. Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275PubMedCrossRefGoogle Scholar
  26. Bullock TH (2000) Revisiting the concept of identifiable neurons. Brain Behav Evol 55:236–240PubMedCrossRefGoogle Scholar
  27. Calman BG, Lauerman MA, Andrews AW, Schmidt M, Battelle BA (1991) Central projections of Limulus photoreceptor cells revealed by a photoreceptor-specific monoclonal antibody. J Comp Neurol 313:553–562PubMedCrossRefGoogle Scholar
  28. Campbell LI, Rota-Stabelli O, Edgecombe GD, Marchioro T, Longhorn SJ, Telford MJ, Philippe H, Rebecchi L, Peterson KJ, Pisani D (2011) MicroRNAs and phylogenomics resolve the relationships of Tardigrada and suggest that velvet worms are the sister group of Arthropoda. Proc Natl Acad Sci USA 108:15920–15924PubMedPubMedCentralCrossRefGoogle Scholar
  29. Carroll SB, Grenier JK, Weatherbee SD (2005) From DNA to diversity. Molecular genetics and the evolution of animal design. Blackwell Publishing, MaldenGoogle Scholar
  30. Castano RA, Castano D, Dewel WC (1996) Arthropod head segmentation: an integrated approach. Am Zool 36:132ACrossRefGoogle Scholar
  31. Chen J, Waloszek D, Maas A (2004) A new “great appendage” arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 37:3–20Google Scholar
  32. Chipman AD, Stollewerk A (2006) Specification of neural precursor identity in the geophilomorph centipede Strigamia maritima. Dev Biol 290:337–350PubMedCrossRefGoogle Scholar
  33. Cong P, Ma X, Hou X, Edgecombe GD, Strausfeld NJ (2014) Brain structure resolves the segmental affinity of anomalocaridid appendages. Nature 513:538–542PubMedCrossRefGoogle Scholar
  34. Damen WGM (2002) Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129:1239–1250PubMedGoogle Scholar
  35. Damen WGM (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236:1379–1391PubMedCrossRefGoogle Scholar
  36. Damen WGM, Hausdorf M, Seyfarth EA, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95:10665–10670PubMedPubMedCentralCrossRefGoogle Scholar
  37. Degma P, Guidetti R (2007) Notes to the current checklist of Tardigrada. Zootaxa 1579:41–53Google Scholar
  38. Degma P, Bertolani R, Guidetti R (2014) Actual checklist of Tardigrada species. Accessed 15 Dec 2016
  39. Deutsch JS (2004) Segments and parasegments in arthropods: a functional perspective. BioEssays 26:1117–1125PubMedCrossRefGoogle Scholar
  40. Dewel RA, Dewel WC (1996) The brain of Echiniscus viridissimus Peterfi, 1956 (Heterotardigrada): a key to understanding the phylogenetic position of tardigrades and the evolution of the arthropod head. Zool J Linn Soc 116:35–49CrossRefGoogle Scholar
  41. Dewel RA, Dewel WC (1997) The place of tardigrades in arthropod evolution. In: Fortey RA, Thomas RH (eds) Arthropod Relationships. Chapman & Hall, London, pp 109–123Google Scholar
  42. Dewel RA, Nelson DR, Dewel WC (1993) Tardigrada. In: Harrison FW, Rice ME (eds) Microscopic anatomy of invertebrates. Wiley, New York, pp 143–183Google Scholar
  43. Dewel RA, Budd GE, Castano DF, Dewel WC (1999) The organization of the suboesophageal nervous system in tardigrades: insights into the evolution of the arthropod hypostome and tritocerebrum. Zool Anz 238:191–203Google Scholar
  44. Doyère M (1840) Mémoire sur les Tardigrades. Ann Sci Nat (Paris) Zool Ser 2 14:269–361Google Scholar
  45. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe GD, Sørensen MV, Haddock SHD, Schmidt-Rhaesa A, Okusu A, Kristensen RM, Wheeler WC, Martindale MQ, Giribet G (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749PubMedCrossRefGoogle Scholar
  46. Eakin RM, Westfall JA (1965) Fine structure of the eye of peripatus (Onychophora). Z Zellforsch Mikrosk Anat 68:278–300PubMedCrossRefGoogle Scholar
  47. Edgecombe GD (2010) Arthropod phylogeny: an overview from the perspectives of morphology, molecular data and the fossil record. Arthropod Struct Dev 39:74–87PubMedCrossRefGoogle Scholar
  48. Edgecombe GD, Ma X, Strausfeld NJ (2015) Unlocking the early fossil record of the arthropod central nervous system. Philos Trans R Soc B Biol Sci 370:20150038CrossRefGoogle Scholar
  49. Eibye-Jacobsen J (1996/1997) New observations on the embryology of the Tardigrada. Zool Anz 235:201–216Google Scholar
  50. Eriksson BJ, Budd GE (2000) Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda. Arthropod Struct Dev 29:197–209PubMedCrossRefGoogle Scholar
  51. Eriksson BJ, Stollewerk A (2010a) The morphological and molecular processes of onychophoran brain development show unique features that are neither comparable to insects nor to chelicerates. Arthropod Struct Dev 39:478–490PubMedCrossRefGoogle Scholar
  52. Eriksson BJ, Stollewerk A (2010b) Expression patterns of neural genes in Euperipatoides kanangrensis suggest divergent evolution of onychophoran and euarthropod neurogenesis. Proc Natl Acad Sci USA 107:22576–22581PubMedPubMedCentralCrossRefGoogle Scholar
  53. Eriksson BJ, Tait NN, Budd GE (2003) Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J Morphol 255:1–23PubMedCrossRefGoogle Scholar
  54. Eriksson BJ, Larson ET, Thörnqvist P-O, Tait NN, Budd GE (2005a) Expression of engrailed in the developing brain and appendages of the onychophoran Euperipatoides kanangrensis (Reid). J Exp Zool Part B Mol Dev Evol 304B:1–9CrossRefGoogle Scholar
  55. Eriksson BJ, Tait NN, Norman JM, Budd GE (2005b) An ultrastructural investigation of the hypocerebral organ of the adult Euperipatoides kanangrensis (Onychophora, Peripatopsidae). Arthropod Struct Dev 34:407–418CrossRefGoogle Scholar
  56. Eriksson BJ, Tait NN, Budd GE, Janssen R, Akam M (2010) Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem. Dev Gene Evol 220:117–122CrossRefGoogle Scholar
  57. Eriksson BJ, Samadi L, Schmid A (2013a) The expression pattern of the genes engrailed, pax6, otd and six3 with special respect to head and eye development in Euperipatoides kanangrensis Reid 1996 (Onychophora: Peripatopsidae). Dev Gene Evol 223:237–246CrossRefGoogle Scholar
  58. Eriksson BJ, Fredman D, Steiner G, Schmid A (2013b) Characterisation and localisation of the opsin protein repertoire in the brain and retinas of a spider and an onychophoran. BMC Evol Biol 13:186PubMedPubMedCentralCrossRefGoogle Scholar
  59. Evans R (1901) On two new species of Onychophora from the Siamese Malay States. Q J Microsc Sci 44:473–538Google Scholar
  60. Fedorow B (1929) Zur Anatomie des Nervensystems von Peripatus. II. Das Nervensystem des vorderen Körperendes und seine Metamerie. Zool Jahrb Abt Anat Ontog Tiere 50:279–332Google Scholar
  61. Fernandez C, Vasanthan T, Kissoon N, Karam G, Duquette N, Seymour C, Stone J (2016) Radiation tolerance and bystander effects in the eutardigrade species Hypsibius dujardini (Parachaela: Hypsibiidae). Zool J Linn Soc 178:919–923CrossRefGoogle Scholar
  62. Feuda R, Hamilton SC, McInerney JO, Pisani D (2012) Metazoan opsin evolution reveals a simple route to animal vision. Proc Natl Acad Sci USA 109:18868–18872PubMedPubMedCentralCrossRefGoogle Scholar
  63. Fortey RA, Thomas RH (1998) Arthropod relationships. Chapman & Hall, LondonCrossRefGoogle Scholar
  64. Franke FA, Mayer G (2014) Controversies surrounding segments and parasegments in Onychophora: insights from the expression patterns of four “segment polarity genes” in the peripatopsid Euperipatoides rowelli. PLoS One 9:e114383PubMedPubMedCentralCrossRefGoogle Scholar
  65. Frase T, Richter S (2013) The fate of the onychophoran antenna. Dev Gene Evol 223:247–251CrossRefGoogle Scholar
  66. Frase T, Richter S (2016) Nervous system development in the fairy shrimp Branchinella sp. (Crustacea: Branchiopoda: Anostraca): insights into the development and evolution of the branchiopod brain and its sensory organs. J Morphol 277:1423–1446PubMedCrossRefGoogle Scholar
  67. Gabriel WN, McNuff R, Patel SK, Gregory TR, Jeck WR, Jones CD, Goldstein B (2007) The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev Biol 312:545–559PubMedCrossRefGoogle Scholar
  68. Gaffron E (1884) Kurzer Bericht über fortgesetze Peripatus-Studien. Zool Anz 7:336–339Google Scholar
  69. Geidies H (1954) Abgeänderte Azan − Methoden. Mikrokosmos 42:239–240Google Scholar
  70. Greeff R (1865) Ueber das Nervensystem der Bärthierchen, Arctiscoida C.A.S. Schultze (Tardigraden Doyère) mit besonderer Berücksichtigung der Muskelnerven und deren Endigungen. Arch mikrosk Anat 1:101–123CrossRefGoogle Scholar
  71. Greven H (2007) Comments on the eyes of tardigrades. Arthropod Struct Dev 36:401–407PubMedCrossRefGoogle Scholar
  72. Greven H, Kuhlmann D (1972) Die Struktur des Nervengewebes von Macrobiotus hufelandi C.A.S. Schultze (Tardigrada). Z Zellforsch 132:131–146PubMedCrossRefGoogle Scholar
  73. Gross V, Mayer G (2015) Neural development in the tardigrade Hypsibius dujardini based on anti-acetylated α-tubulin immunolabeling. EvoDevo 6:12PubMedPubMedCentralCrossRefGoogle Scholar
  74. Gross V, Treffkorn S, Mayer G (2015) Tardigrada. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates. Springer, Berlin, pp 35–52CrossRefGoogle Scholar
  75. Guidetti R, Bertolani R (2005) Tardigrade taxonomy: an updated check list of the taxa and a list of characters for their identification. Zootaxa 845:1–46CrossRefGoogle Scholar
  76. Guilding L (1826) Mollusca caribbaeana. Zool J 2:437–449Google Scholar
  77. Halberg KA, Jørgensen A, Møbjerg N (2013) Desiccation tolerance in the tardigrade Richtersius coronifer relies on muscle mediated structural reorganization. PLoS One 8:e85091PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hanström B (1928) Onychophora. Vergleichende Anatomie des Nervensystems der Wirbellosen Tiere unter Berücksichtigung seiner Funktion. Springer, Berlin, pp 341–351Google Scholar
  79. Hanström B (1935) Bemerkungen über das Gehirn und die Sinnesorgane der Onychophoren. Lund Univ Årsskr 31:1–37Google Scholar
  80. Harrison PJ, Macmillan DL, Young HM (1995) Serotonin immunoreactivity in the ventral nerve cord of the primitive crustacean Anaspides tasmaniae closely resembles that of crayfish. J Exp Biol 198:531–535PubMedGoogle Scholar
  81. Harzsch S (2003) 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 258:44–56PubMedCrossRefGoogle Scholar
  82. Harzsch S (2004a) Phylogenetic comparison of serotonin-immunoreactive neurons in representatives of the Chilopoda, Diplopoda, and Chelicerata: implications for arthropod relationships. J Morphol 259:198–213PubMedCrossRefGoogle Scholar
  83. Harzsch S (2004b) The tritocerebrum of Euarthropoda: a “non-drosophilocentric” perspective. Evol Dev 6:303–309PubMedCrossRefGoogle Scholar
  84. Harzsch S (2006) Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny. Integr Comp Biol 46:162–194PubMedCrossRefGoogle Scholar
  85. Harzsch S, Waloszek D (2000) Serotonin-immunoreactive neurons in the ventral nerve cord of Crustacea: a character to study aspects of arthropod phylogeny. Arthropod Struct Dev 29:307–322PubMedCrossRefGoogle Scholar
  86. Harzsch S, Wildt M, Battelle B, Waloszek D (2005) Immunohistochemical localization of neurotransmitters in the nervous system of larval Limulus polyphemus (Chelicerata, Xiphosura): evidence for a conserved protocerebral architecture in Euarthropoda. Arthropod Struct Dev 34:327–342CrossRefGoogle Scholar
  87. Harzsch S, Sandeman D, Chaigneau J (2006) Morphology and development of the central nervous system. Koninklijke Brill Academic Publishers, Leiden, pp 1–84Google Scholar
  88. Hashimoto T, Horikawa DD, Saito Y, Kuwahara H, Kozuka-Hata H, Shin-I T, Minakuchi Y, Ohishi K, Motoyama A, Aizu T, Enomoto A, Kondo K, Tanaka S, Hara Y, Koshikawa S, Sagara H, Miura T, Yokobori S, Miyagawa K, Suzuki Y, Kubo T, Oyama M, Kohara Y, Fujiyama A, Arakawa K, Katayama T, Toyoda A, Kunieda T (2016) Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nat Commun 7:12808PubMedPubMedCentralCrossRefGoogle Scholar
  89. Haug JT, Waloszek D, Maas A, Liu Y, Haug C (2012) Functional morphology, ontogeny and evolution of mantis shrimp-like predators in the Cambrian. Palaeontology 55:369–399CrossRefGoogle Scholar
  90. Heidemann NW, Smith DK, Hygum TL, Stapane L, Clausen LK, Jørgensen A, Hélix-Nielsen C, Møbjerg N (2016) Osmotic stress tolerance in semi-terrestrial tardigrades. Zool J Linn Soc 178:912–918CrossRefGoogle Scholar
  91. Heidenhain M (1915) Über die mallorysche Bindegewebsfärbung mit Karmin und Azokarmin als Vorfarben. Z Wiss Mikrosk 33:361–372Google Scholar
  92. Hejnol A, Lowe CJ (2015) Embracing the comparative approach: how robust phylogenies and broader developmental sampling impacts the understanding of nervous system evolution. Philos Trans R Soc B Biol Sci 370:20150045CrossRefGoogle Scholar
  93. Hejnol A, Schnabel R (2005) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361PubMedCrossRefGoogle Scholar
  94. Hejnol A, Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguñà J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenomic methods. Proc R Soc B Biol Sci 276:4261–4270CrossRefGoogle Scholar
  95. Hengherr S, Heyer AG, Köhler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades—evidence for divergence in responses to dehydration. FEBS J 275:281–288PubMedCrossRefGoogle Scholar
  96. Henry LM (1948) The nervous system and the segmentation of the head in the Annulata. Microentomology 13:27–48PubMedGoogle Scholar
  97. Henze MJ, Oakley TH (2015) The dynamic evolutionary history of pancrustacean eyes and opsins. Integr Comp Biol 55:830–842PubMedCrossRefGoogle Scholar
  98. Hering L, Mayer G (2014) Analysis of the opsin repertoire in the tardigrade Hypsibius dujardini provides insights into the evolution of opsin genes in Panarthropoda. Genome Biol Evol 6:2380–2391PubMedPubMedCentralCrossRefGoogle Scholar
  99. Hering L, Henze MJ, Kohler M, Kelber A, Bleidorn C, Leschke M, Nickel B, Meyer M, Kircher M, Sunnucks P, Mayer G (2012) Opsins in Onychophora (velvet worms) suggest a single origin and subsequent diversification of visual pigments in arthropods. Mol Biol Evol 29:3451–3458PubMedCrossRefGoogle Scholar
  100. Hering L, Bouameur J-E, Reichelt J, Magin TM, Mayer G (2016) Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades. eLife 5:e11117PubMedPubMedCentralCrossRefGoogle Scholar
  101. Hermans CO, Eakin RM (1974) Fine structure of the eyes of an alciopid polychaete, Vanadis tagensis (Annelida). Z Morphol Tiere 79:245–267Google Scholar
  102. Heymons R (1901) Die Entwicklungsgeschichte der Scolopender. Zoologica 33:1–244Google Scholar
  103. Hochberg R, Litvaitis MK (2003) Ultrastructural and immunocytochemical observations of the nervous systems of three macrodasyidan gastrotrichs. Acta Zool 84:171–178CrossRefGoogle Scholar
  104. Holmgren NF (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden, und Insekten. Vorstudien zu einer Phylogenie der Arthropoden. Kungl Svenska Vetenskapsakad Handlingar [Ser 2] 56:1–303Google Scholar
  105. Homberg U (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37:347–362PubMedCrossRefGoogle Scholar
  106. Hou XG, Ma XY, Zhao J, Bergström J (2004) The lobopodian Paucipodia inermis from the Lower Cambrian Chengjiang fauna, Yunnan, China. Lethaia 37:235–244CrossRefGoogle Scholar
  107. Hoyle G (1983) On the way to neuroethology: the identified neuron approach. Neuroethology and behavioral physiology. Springer, New York, pp 9–25CrossRefGoogle Scholar
  108. Ingham P, Martinez Arias A (1992) Boundaries and fields in early embryos. Cell 68:221–235PubMedCrossRefGoogle Scholar
  109. Janssen R (2017) Comparative analysis of gene expression patterns in the arthropod labrum and the onychophoran frontal appendages, and its implications for the arthropod head problem. EvoDevo 8:1PubMedPubMedCentralCrossRefGoogle Scholar
  110. Jönsson KI (2001) The nature of selection on anhydrobiotic capacity in tardigrades. Zool Anz 240:409–417CrossRefGoogle Scholar
  111. Kashiyama K, Seki T, Numata H, Goto SG (2009) Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda. Mol Biol Evol 26:299–311PubMedCrossRefGoogle Scholar
  112. Katti C, Kempler K, Porter ML, Legg A, Gonzalez R, Garcia-Rivera E, Dugger D, Battelle B-A (2010) Opsin co-expression in Limulus photoreceptors: differential regulation by light and a circadian clock. J Exp Biol 213:2589–2601PubMedPubMedCentralCrossRefGoogle Scholar
  113. Kimm MA, Prpic NM (2006) Formation of the arthropod labrum by fusion of paired and rotated limb-bud-like primordia. Zoomorphology 125:147–155CrossRefGoogle Scholar
  114. Kinchin IM (1994) The biology of Tardigrades. Portland Press Inc., LondonGoogle Scholar
  115. Kirsch R, Richter S (2007) The nervous system of Leptodora kindtii (Branchiopoda, Cladocera) surveyed with Confocal Scanning Microscopy (CLSM), including general remarks on the branchiopod neuromorphological ground pattern. Arthropod Struct Dev 36:143–156PubMedCrossRefGoogle Scholar
  116. Kotikova EA (1995) Localization and neuroanatomy of catecholaminergic neurons in some rotifer species. Hydrobiologia 313(314):123–127CrossRefGoogle Scholar
  117. Koutsovoulos G, Kumar S, Laetsch DR, Stevens L, Daub J, Conlon C, Maroon H, Thomas F, Aboobaker AA, Blaxter M (2016) No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc Natl Acad Sci USA 113:5053–5058PubMedPubMedCentralCrossRefGoogle Scholar
  118. Koyanagi M, Nagata T, Katoh K, Yamashita S, Tokunaga F (2008) Molecular evolution of arthropod color vision deduced from multiple opsin genes of jumping spiders. J Mol Evol 66:130–137PubMedCrossRefGoogle Scholar
  119. Kristensen RM (1978) Notes on marine Heterotardigrades l. Description of two new Batillipes species, using the electron microscope. Zool Anz 200:1–17Google Scholar
  120. Kristensen RM (1983) The first record of cyclomorphosis in Tardigrada based on a new genus and species from Arctic meiobenthos. Z Zool Syst Evolutionsforsch 20:249–270CrossRefGoogle Scholar
  121. Kutsch W, Breidbach O (1994) Homologues structures in the nervous system of Arthropoda. Adv Insect Physiol 24:1–113CrossRefGoogle Scholar
  122. Land MF, Nilsson D-E (2012) Animal eyes. Oxford University Press, OxfordCrossRefGoogle Scholar
  123. Legg DA, Vannier J (2013) The affinities of the cosmopolitan arthropod Isoxys and its implications for the origin of arthropods. Lethaia 46:540–550CrossRefGoogle Scholar
  124. Legg DA, Sutton MD, Edgecombe GD, Caron J-B (2012) Cambrian bivalved arthropod reveals origin of arthrodization. Proc R Soc B Biol Sci 279:4699–4704CrossRefGoogle Scholar
  125. Legg DA, Sutton MD, Edgecombe GD (2013) Arthropod fossil data increase congruence of morphological and molecular phylogenies. Nat Commun 4:2485PubMedCrossRefGoogle Scholar
  126. Lehmann T, Heß M, Melzer RR (2012) Wiring a periscope—ocelli, retinula axons, visual neuropils and the ancestrality of sea spiders. PLoS One 7:e30474PubMedPubMedCentralCrossRefGoogle Scholar
  127. Liu J, Shu D, Han J, Zhang Z (2004) A rare lobopod with well-preserved eyes from Chengjiang Lagerstätte and its implications for origin of arthropods. Chin Sci Bull 49:1063–1071CrossRefGoogle Scholar
  128. Loesel R, Wolf H, Kenning M, Harzsch S, Sombke A (2013) Architectural principles and evolution of the arthropod central nervous system. In: Minelli A, Boxshall G, Fusco G (eds) Arthropod biology and evolution—molecules, development, morphology. Springer, Heidelberg, pp 299–342CrossRefGoogle Scholar
  129. Mallatt J, Giribet G (2006) Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Biol Evol 40:772–794Google Scholar
  130. Mallatt JM, Garey JR, Shultz 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 31:178–191PubMedCrossRefGoogle Scholar
  131. Marcus E (1929) Tardigrada. In: Bronn HG (ed) Klassen und Ordnungen des Tierreichs. Akademische Verlagsgesellschaft, Leipzig, pp 1–609Google Scholar
  132. Martin C, Mayer G (2014) Neuronal tracing of oral nerves in a velvet worm—implications for the evolution of the ecdysozoan brain. Front Neuroanat 8(7):1–13Google Scholar
  133. Martin C, Mayer G (2015) Insights into the segmental identity of post-oral commissures and pharyngeal nerves in Onychophora based on retrograde fills. BMC Neurosci 16:53PubMedPubMedCentralCrossRefGoogle Scholar
  134. Martin C, Gross V, Pflüger H-J, Stevenson PA, Mayer G (2017) Assessing segmental versus non-segmental features in the ventral nervous system of onychophorans (velvet worms). BMC Evol Biol 17:3PubMedPubMedCentralCrossRefGoogle Scholar
  135. Mayer G (2006) Structure and development of onychophoran eyes—what is the ancestral visual organ in arthropods? Arthropod Struct Dev 35:231–245PubMedCrossRefGoogle Scholar
  136. Mayer G (2016) Onychophora. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 390–401Google Scholar
  137. Mayer G, Harzsch S (2007) Immunolocalization of serotonin in Onychophora argues against segmental ganglia being an ancestral feature of arthropods. BMC Evol Biol 7:118PubMedPubMedCentralCrossRefGoogle Scholar
  138. Mayer G, Harzsch S (2008) Distribution of serotonin in the trunk of Metaperipatus blainvillei (Onychophora, Peripatopsidae): implications for the evolution of the nervous system in Arthropoda. J Comp Neurol 507:1196–1208PubMedCrossRefGoogle Scholar
  139. Mayer G, Koch M (2005) Ultrastructure and fate of the nephridial anlagen in the antennal segment of Epiperipatus biolleyi (Onychophora, Peripatidae)—evidence for the onychophoran antennae being modified legs. Arthropod Struct Dev 34:471–480CrossRefGoogle Scholar
  140. Mayer G, Oliveira IS (2011) Phylum Onychophora Grube, 1853. In: Zhang Z-Q (ed) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:98Google Scholar
  141. Mayer G, Oliveira IS (2013) Phylum Onychophora Grube, 1853. In: Zhang Z-Q (ed) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness (Addenda 2013). Zootaxa 3703:15–16Google Scholar
  142. Mayer G, Whitington PM (2008) Insights into neural anatomy and development in Onychophora. J Morphol 269:1463–1464Google Scholar
  143. Mayer G, Whitington PM (2009a) Neural development in Onychophora (velvet worms) suggests a step-wise evolution of segmentation in the nervous system of Panarthropoda. Dev Biol 335:263–275PubMedCrossRefGoogle Scholar
  144. Mayer G, Whitington PM (2009b) Velvet worm development links myriapods with chelicerates. Proc R Soc B Biol Sci 276:3571–3579CrossRefGoogle Scholar
  145. Mayer G, Bartolomaeus T, Ruhberg H (2005) Ultrastructure of mesoderm in embryos of Opisthopatus roseus (Onychophora, Peripatopsidae): revision of the “long germ band” hypothesis for Opisthopatus. J Morphol 263:60–70PubMedCrossRefGoogle Scholar
  146. Mayer G, Whitington PM, Sunnucks P, Pflüger H-J (2010) A revision of brain composition in Onychophora (velvet worms) suggests that the tritocerebrum evolved in arthropods. BMC Evol Biol 10:255PubMedPubMedCentralCrossRefGoogle Scholar
  147. Mayer G, Martin C, Rüdiger J, Kauschke S, Stevenson PA, Poprawa I, Hohberg K, Schill RO, Pflüger H-J, Schlegel M (2013a) Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods. BMC Evol Biol 13:230PubMedPubMedCentralCrossRefGoogle Scholar
  148. Mayer G, Kauschke S, Rüdiger J, Stevenson PA (2013b) Neural markers reveal a one-segmented head in tardigrades (water bears). PLoS One 8:e59090PubMedPubMedCentralCrossRefGoogle Scholar
  149. Mayer G, Martin C, de Sena OI, Franke FA, Gross V (2014) Latest anomalocaridid affinities challenged. Nature 516:E1–E2PubMedCrossRefGoogle Scholar
  150. Mayer G, Oliveira IS, Baer A, Hammel JU, Gallant J, Hochberg R (2015a) Capture of prey, feeding, and functional anatomy of the jaws in velvet worms (Onychophora). Integr Comp Biol 55:217–227PubMedCrossRefGoogle Scholar
  151. Mayer G, Hering L, Stosch JM, Stevenson PA, Dircksen H (2015b) Evolution of pigment-dispersing factor neuropeptides in Panarthropoda: insights from Onychophora (velvet worms) and Tardigrada (water bears). J Comp Neurol 523:1865–1885PubMedCrossRefGoogle Scholar
  152. Mayer G, Franke FA, Treffkorn S, Oliveira I (2015c) Onychophora. In: Wanninger A (ed) Evolutionary developmental biology of invertebrates. Springer, Berlin, pp 53–98CrossRefGoogle Scholar
  153. Minelli A, Boxshall G, Fusco G (2013) Arthropod biology and evolution: molecules, development, morphology. Springer Science & Business MediaGoogle Scholar
  154. Mittmann B, Scholtz G (2003) Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev Gene Evol 213:9–17Google Scholar
  155. Mittmann B, Wolff C (2012) Embryonic development and staging of the cobweb spider Parasteatoda tepidariorum C. L. Koch, 1841 (syn.: Achaearanea tepidariorum; Araneomorphae; Theridiidae). Dev Gene Evol 222:189–216CrossRefGoogle Scholar
  156. Mizunami M, Iwasaki M, Okada R, Nishikawa M (1998) Topography of four classes of Kenyon cells in the mushroom bodies of the cockroach. J Comp Neurol 399:162–175PubMedCrossRefGoogle Scholar
  157. Møbjerg N, Halberg KA, Jørgensen A, Persson D, Bjørn M, Ramløv H, Kristensen RM (2011) Survival in extreme environments—on the current knowledge of adaptations in tardigrades. Acta Physiol 202:409–420CrossRefGoogle Scholar
  158. Müller MCM, Westheide W (2002) Comparative analysis of the nervous systems in presumptive progenetic dinophilid and dorvilleid polychaetes (Annelida) by immunohistochemistry and cLSM. Acta Zool 83:33–48CrossRefGoogle Scholar
  159. Murienne J, Daniels SR, Buckley TR, Mayer G, Giribet G (2014) A living fossil tale of Pangean biogeography. Proc R Soc B Biol Sci 281:1471–2954Google Scholar
  160. Nelson DR, Guidetti R, Rebecchi L (2015) Phylum Tardigrada. In: Thorp J, Rogers DC (eds) Ecology and general biology: Thorp and Covich’s freshwater invertebrates. Academic Press, Cambridge, pp 347–380CrossRefGoogle Scholar
  161. Nielsen C (2012) Animal evolution: interrelationships of the living phyla. Oxford University Press, OxfordGoogle Scholar
  162. Nilsson D-E (2013) Eye evolution and its functional basis. Vis Neurosci 30:5–20PubMedPubMedCentralCrossRefGoogle Scholar
  163. Niven JE, Farris SM (2012) Miniaturization of nervous systems and neurons. Curr Biol 22:R323–R329PubMedCrossRefGoogle Scholar
  164. Northcutt RG (2012) Evolution of centralized nervous systems: two schools of evolutionary thought. Proc Natl Acad Sci USA 109:10626–10633PubMedPubMedCentralCrossRefGoogle Scholar
  165. Oliveira IS, Mayer G (2013) Apodemes associated with limbs support serial homology of claws and jaws in Onychophora (velvet worms). J Morphol 274:1180–1190CrossRefGoogle Scholar
  166. Oliveira IS, Lacorte GA, Fonseca CG, Wieloch AH, Mayer G (2011) Cryptic speciation in Brazilian Epiperipatus (Onychophora: Peripatidae) reveals an underestimated diversity among the peripatid velvet worms. PLoS One 6:e19973PubMedPubMedCentralCrossRefGoogle Scholar
  167. Oliveira IS, Franke FA, Hering L, Schaffer S, Rowell DM, Weck-Heimann A, Monge-Nájera J, Morera-Brenes B, Mayer G (2012) Unexplored character diversity in Onychophora (velvet worms): a comparative study of three peripatid species. PLoS One 7:e51220PubMedCentralCrossRefGoogle Scholar
  168. Oliveira IS, Tait NN, Strübing I, Mayer G (2013) The role of ventral and preventral organs as attachment sites for segmental limb muscles in Onychophora. Front Zool 10:73CrossRefGoogle Scholar
  169. Oliveira IS, Bai M, Jahn H, Gross V, Martin C, Hammel JU, Zhang W, Mayer G (2016) Earliest onychophoran in amber reveals Gondwanan migration patterns. Curr Biol 26:2594–2601PubMedCrossRefGoogle Scholar
  170. Ortega-Hernández J, Budd GE (2016) The nature of non-appendicular anterior paired projections in Palaeozoic total-group Euarthropoda. Arthropod Struct Dev 45:185–199PubMedCrossRefGoogle Scholar
  171. Ortega-Hernández J, Janssen R, Budd GE (2017) Origin and evolution of the panarthropod head–A palaeobiological and developmental perspective. Arthropod Struct Dev 46:354–379PubMedCrossRefGoogle Scholar
  172. Osorio D, Averof M, Bacon JP (1995) Arthropod evolution: great brains, beautiful bodies. Trends Ecol Evol 10:449–454PubMedCrossRefGoogle Scholar
  173. Ou Q, Shu D, Mayer G (2012) Cambrian lobopodians and extant onychophorans provide new insights into early cephalization in Panarthropoda. Nat Commun 3:1261PubMedPubMedCentralCrossRefGoogle Scholar
  174. Paterson JR, García-Bellido DC, Lee MSY, Brock GA, Jago JB, Edgecombe GD (2011) Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480:237–240PubMedCrossRefGoogle Scholar
  175. Paulus HF (1979) Eye structure and the monophyly of the Arthropoda. In: Gupta AP (ed) Arthropod phylogeny. Van Nostrand Reinhold Company, New York, pp 299–383Google Scholar
  176. Paulus HF (2000) Phylogeny of the Myriapoda–Crustacea–Insecta: a new attempt using photoreceptor structure. J Zool Syst Evol Res 38:189–208CrossRefGoogle Scholar
  177. Persson DK, Halberg KA, Jørgensen A, Møbjerg N, Kristensen RM (2012) Neuroanatomy of Halobiotus crispae (Eutardigrada: Hypsibiidae): tardigrade brain structure supports the clade Panarthropoda. J Morphol 273:1227–1245PubMedCrossRefGoogle Scholar
  178. Persson DK, Halberg KA, Jørgensen A, Møbjerg N, Kristensen RM (2014) Brain anatomy of the marine tardigrade Actinarctus doryphorus (Arthrotardigrada). J Morphol 275:173–190PubMedCrossRefGoogle Scholar
  179. Petrof I, Sherman SM (2013) Functional significance of synaptic terminal size in glutamatergic sensory pathways in thalamus and cortex. J Physiol 591:3125–3131PubMedPubMedCentralCrossRefGoogle Scholar
  180. Pflüger HJ, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396CrossRefGoogle Scholar
  181. Pflugfelder O (1948) Entwicklung von Paraperipatus amboinensis n. sp. Zool Jahrb Abt Anat Ontog Tiere 69:443–492Google Scholar
  182. Plachetzki DC, Degnan BM, Oakley TH (2007) The origins of novel protein interactions during animal opsin evolution. PLoS One 2(10):e1054PubMedPubMedCentralCrossRefGoogle Scholar
  183. Poinar G (2000) Fossil onychophorans from Dominican and Baltic amber: Tertiapatus dominicanus n.g., n.sp. (Tertiapatidae n.fam.) and Succinipatopsis balticus n.g., n.sp. (Succinipatopsidae n.fam.) with a proposed classification of the subphylum Onychophora. Invertebr Biol 119:104–109CrossRefGoogle Scholar
  184. Porter ML, Cronin TW, McClellan DA, Crandall KA (2007) Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Mol Biol Evol 24:253–268PubMedCrossRefGoogle Scholar
  185. Porter ML, Blasic JR, Bok MJ, Cameron EG, Pringle T, Cronin TW, Robinson PR (2012) Shedding new light on opsin evolution. Proc R Soc B 279:3–14PubMedCrossRefGoogle Scholar
  186. Prpic N-M, Wigand B, Damen WG, Klingler M (2001) Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Gene Evol 211:467–477CrossRefGoogle Scholar
  187. Purschke G (2016) Annelida: basal groups and Pleistoannelida. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford Univesity Press, Oxford, pp 254–312Google Scholar
  188. Ramirez MD, Pairett AN, Pankey MS, Serb JM, Speiser DI, Swafford AJ, Oakley TH (2016) The last common ancestor of most bilaterian animals possessed at least nine opsins. Genome Biol Evol 8:3640–3652PubMedPubMedCentralCrossRefGoogle Scholar
  189. Ramløv H, Westh P (2001) Cryptobiosis in the eutardigrade Adorybiotus (Richtersius) coronifer: tolerance to alcohols, temperature and de novo protein synthesis. Zool Anz 240:517–523CrossRefGoogle Scholar
  190. Rebecchi L, Altiero T, Cesari M, Bertolani R, Rizzo AM, Corsetto PA, Guidetti R (2011) Resistance of the anhydrobiotic eutardigrade Paramacrobiotus richtersi to space flight (LIFE–TARSE mission on FOTON-M3). J Zool Syst Evol Res 49(Suppl. 1):98–103CrossRefGoogle Scholar
  191. Rehm P, Borner J, Meusemann K, von Reumont BM, Simon S, Hadrys H, Misof B, Burmester T (2011) Dating the arthropod tree based on large-scale transcriptome data. Mol Phylogenet Evol 61:880–887PubMedCrossRefGoogle Scholar
  192. Reisinger E (1925) Untersuchungen am Nervensystem der Bothrioplana semperi Braun. (Zugleich ein Beitrag zur Technik der vitalen Nervenfärbung und zur vergleichenden Anatomie des Plathelminthennervensystems.). Z Morph Ökol Tiere 5:119–149CrossRefGoogle Scholar
  193. Reisinger E (1972) Die evolution des Orthogons der Spiralier und das Archicölomatenproblem. Z Zool Syst Evolutionsforsch 10:1–43CrossRefGoogle Scholar
  194. Reuter M, Mäntylä K, Gustafsson MKS (1998) Organization of the orthogon—main and minor nerve cords. Hydrobiologia 383:175–182CrossRefGoogle Scholar
  195. Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Döring C, Faller S, Fritsch M, Grobe P, Heuer CM, Kaul S, Møller OS, Müller CHG, Rieger V, Rothe BH, Stegner MEJ, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29PubMedPubMedCentralCrossRefGoogle Scholar
  196. Richter S, Stein M, Frase T, Szucsich NU (2013) The arthropod head. In: Minelli A, Boxshall G, Fusco G (eds) Arthropod biology and evolution. Springer, Heidelberg, pp 223–240CrossRefGoogle Scholar
  197. Rogers BT, Kaufman TC (1997) Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. Int Rev Cytol 174:1–84PubMedCrossRefGoogle Scholar
  198. Rota-Stabelli O, Kayal E, Gleeson D, Daub J, Boore J, Telford M, Pisani D, Blaxter M, Lavrov D (2010) Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biol Evol 2:425–440PubMedPubMedCentralCrossRefGoogle Scholar
  199. Rota-Stabelli O, Daley AC, Pisani D (2013) Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr Biol 23:1–7CrossRefGoogle Scholar
  200. Rothe BH, Schmidt-Rhaesa A (2010) Structure of the nervous system in Tubiluchus troglodytes (Priapulida). Invertebr Biol 129:39–58CrossRefGoogle Scholar
  201. Ruhberg H, Mayer G (2013) Onychophora, Stummelfüßer. In: Westheide W, Rieger G (eds) Spezielle Zoologie Teil 1: Einzeller und Wirbellose Tiere. Springer, Berlin, pp 457–464Google Scholar
  202. Ruhberg H, Tiemann H, Mette A, Rhode B (2001) Evolutionäre Aspekte der Augen-Rückbildung beim hemiedaphischen Onychophoren Tasmanipatus anophthalmus Ruhberg et al., 1991 (Peripatopsidae). Mitt Hambg Zool Mus Inst 98:31–50Google Scholar
  203. Sanchez S (1958) Cellules neurosécrétrices et organes infracérébraux de Peripatopsis moseleyi Wood (Onychophores) et neurosécrétion chez Nymphon gracile Leach (Pycnogonides). Arch Zool Exp Gene Notes Rev 96:57–62Google Scholar
  204. Schmidt-Rhaesa A (2001) Tardigrades—Are they really miniaturized dwarfs? Zool Anz 240:549–555CrossRefGoogle Scholar
  205. Schmidt-Rhaesa A (2007) The evolution of organ systems. Oxford University Press, OxfordCrossRefGoogle Scholar
  206. Schmidt-Rhaesa A, Henne S (2016) Cycloneuralia (Nematoda, Nematomorpha, Priapulida, Kinorhyncha, Loricifera). In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 368–381Google Scholar
  207. Schmidt-Rhaesa A, Harzsch S, Purschke G (2016) Structure and evolution of invertebrate nervous systems. Oxford University Press, OxfordGoogle Scholar
  208. Schoenemann B, Liu JN, Shu DG, Han J, Zhang ZF (2009) A miniscule optimized visual system in the lower Cambrian. Lethaia 42:265–273CrossRefGoogle Scholar
  209. Schokraie E, Hotz-Wagenblatt A, Warnken U, Frohme M, Dandekar T, Schill RO, Schnölzer M (2011) Investigating heat shock proteins of tardigrades in active versus anhydrobiotic state using shotgun proteomics. J Zool Syst Evol Res 49(Suppl. 1):111–119CrossRefGoogle Scholar
  210. Scholtz G (2002) The Articulata hypothesis—or what is a segment? Org Divers Evol 2:197–215CrossRefGoogle Scholar
  211. Scholtz G (2016) Perspective—heads and brains in arthropods: 40 years after the’endless dispute’. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 402–410Google Scholar
  212. Scholtz G, Edgecombe GD (2005) Heads, Hox and the phylogenetic position of trilobites. In: Koenemann S, Jenner RA (eds) Crustacea and arthropod relationship. CRC Press, Boca Raton, FL, pp 139–165Google Scholar
  213. Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Gene Evol 216:395–415CrossRefGoogle Scholar
  214. Schulze C, Persson D (2016) Tardigrada. In: Schmidt-Rhaesa A, Harzsch S, Purschke G (eds) Structure and evolution of invertebrate nervous systems. Oxford University Press, Oxford, pp 383–389Google Scholar
  215. Schulze C, Neves RC, Schmidt-Rhaesa A (2014) Comparative immunohistochemical investigation on the nervous system of two species of Arthrotardigrada (Heterotardigrada, Tardigrada). Zool Anz 253:225–235CrossRefGoogle Scholar
  216. Schumann I, Hering L, Mayer G (2016) Immunolocalization of Arthropsin in the onychophoran Euperipatoides rowelli (Peripatopsidae). Front Neuroanat 10:80PubMedPubMedCentralCrossRefGoogle Scholar
  217. Schürmann FW (1987) Histology and ultrastructure of the onychophoran brain. In: Gupta AP (ed) Arthropod brain, its evolution, development, structure, and functions. Wiley, New York, pp 159–180Google Scholar
  218. Schürmann FW (1995) Common and special features of the nervous system of Onychophora: a comparison with Arthropoda, Annelida and some other invertebrates. In: Breidbach O, Kutsch W (eds) The nervous system of invertebrates: an evolutionary and comparative approach. Birkhäuser, Basel, pp 139–158CrossRefGoogle Scholar
  219. Schürmann FW, Sandeman DC (1976) Giant fibres in the ventral nerve cord of Peripatoides leuckarti (Onychophora). Naturwissenschaften 63:580–581PubMedCrossRefGoogle Scholar
  220. Sedgwick A (1885) The development of Peripatus capensis. Proc R Soc Lond B Biol Sci 38:354–361CrossRefGoogle Scholar
  221. Sedgwick A (1887) The development of the Cape species of peripatus. Part III. On the changes from stage A to stage F. Q J Microsc Sci 27:467–550Google Scholar
  222. Sedgwick A (1895) Peripatus. In: Harmer SF, Shipley AE (eds) Peripatus, Myriapods and Insects, part I. MacMillan & Co., London, pp 3–26Google Scholar
  223. Shichida Y, Matsuyama T (2009) Evolution of opsins and phototransduction. Philos Trans R Soc B Biol Sci 364:2881–2895CrossRefGoogle Scholar
  224. Simonnet F, Deutsch J, Quéinnec E (2004) Hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev Gene Evol 214:537–545CrossRefGoogle Scholar
  225. Skeath JB, Panganiban G, Selegue J, Carroll SB (1992) Gene regulation in two dimensions: the proneural achaete and scute genes are controlled by combinations of axis-patterning genes through a common intergenic control region. Gene Dev 6:2606–2619PubMedCrossRefGoogle Scholar
  226. Smith FW, Goldstein B (2017) Segmentation in Tardigrada and diversification of segmental patterns in Panarthropoda. Arthropod Struct Dev 46:328–340PubMedCrossRefGoogle Scholar
  227. Smith FW, Jockusch EL (2014) The metameric pattern of Hypsibius dujardini (Eutardigrada) and its relationship to that of other panarthropods. Front Zool 11:66CrossRefGoogle Scholar
  228. Smith MR, Ortega-Hernández J (2014) Hallucigenia’s onychophoran-like claws and the case for Tactopoda. Nature 514:363–366PubMedCrossRefGoogle Scholar
  229. Smith FW, Boothby TC, Giovannini I, Rebecchi L, Jockusch EL, Goldstein B (2016) The compact body plan of tardigrades evolved by the loss of a large body region. Curr Biol 26:224–229PubMedCrossRefGoogle Scholar
  230. Stegner ME, Brenneis G, Richter S (2014) The ventral nerve cord in Cephalocarida (Crustacea): new insights into the ground pattern of Tetraconata. J Morphol 275:269–294PubMedCrossRefGoogle Scholar
  231. Stein M (2010) A new arthropod from the Early Cambrian of North Greenland, with a ‘great appendage’-like antennula. Zool J Linn Soc 158:477–500CrossRefGoogle Scholar
  232. 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 328:63–75PubMedCrossRefGoogle Scholar
  233. Strausfeld NJ, Strausfeld C, Stowe S, Rowell D, Loesel R (2006a) The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli. Arthropod Struct Dev 35:169–196PubMedCrossRefGoogle Scholar
  234. Strausfeld NJ, Strausfeld CM, Loesel R, Rowell D, Stowe S (2006b) Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc R Soc Biol Sci Ser B 273:1857–1866CrossRefGoogle Scholar
  235. Strausfeld NJ, Ma X, Edgecombe GD (2016) Fossils and the evolution of the arthropod brain. Curr Biol 26:R989–R1000PubMedCrossRefGoogle Scholar
  236. Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95:10671–10675PubMedPubMedCentralCrossRefGoogle Scholar
  237. Tiegs OW (1940) The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q J Microsc Sci 82:1–225Google Scholar
  238. Tiegs OW (1947) The development and affinities of the Pauropoda, based on a study of Pauropus silvaticus. Part I. Q J Microsc Sci 88:165–267PubMedGoogle Scholar
  239. Tsujimoto M, Imura S, Kanda H (2016) Recovery and reproduction of an Antarctic tardigrade retrieved from a moss sample frozen for over 30 years. Cryobiology 72:78–81PubMedCrossRefGoogle Scholar
  240. Ungerer P, Wolff C (2005) External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89–99CrossRefGoogle Scholar
  241. von Kennel J (1888) Entwicklungsgeschichte von Peripatus edwardsii Blanch. und Peripatus torquatus n. sp. II. Theil. Arb Zool Zootom Inst Würzburg 8:1–93Google Scholar
  242. Vopalensky P, Kozmik Z (2009) Eye evolution: common use and independent recruitment of genetic components. Philos Trans R Soc B Biol Sci 364:2819–2832CrossRefGoogle Scholar
  243. Walker MH, Tait NN (2004) Studies on embryonic development and the reproductive cycle in ovoviviparous Australian Onychophora (Peripatopsidae). J Zool 264:333–354CrossRefGoogle Scholar
  244. Waloszek D, Chen J, Maas A, Wang X (2005) Early Cambrian arthropods—new insights into arthropod head and structural evolution. Arthropod Struct Dev 34:189–205CrossRefGoogle Scholar
  245. Whitington PM (2007) The evolution of arthropod nervous systems: insights from neural development in the Onychophora and Myriapoda. In: Striedter GF, Rubenstein JLR (eds) Theories, development, invertebrates. Academic Press, Oxford, pp 317–336Google Scholar
  246. Whitington PM, Bacon JP (1997) The organization and development of the arthropod ventral nerve cord: insight into arthropod relationships. In: RA F, RH T (eds) Arthropod Relationships. Chapman & Hall, London, pp 349–367Google Scholar
  247. Whitington P, Mayer G (2011) The origins of the arthropod nervous system: insights from the Onychophora. Arthropod Struct Dev 40:193–209PubMedCrossRefGoogle Scholar
  248. Wiederhöft H, Greven H (1999) Notes on head sensory organs of Milnesium tardigradum Doyère, 1840 (Apochela, Eutardigrada). Zool Anz 238:338–346Google Scholar
  249. Yang J, Ortega-Hernández J, Butterfield NJ, Liu Y, Boyan GS, J-b H, Lan T, X-g Z (2016) Fuxianhuiid ventral nerve cord and early nervous system evolution in Panarthropoda. Proc Natl Acad Sci USA 113:2988–2993PubMedPubMedCentralCrossRefGoogle Scholar
  250. Zantke J, Wolff C, Scholtz G (2008) Three-dimensional reconstruction of the central nervous system of Macrobiotus hufelandi (Eutardigrada, Parachela): implications for the phylogenetic position of Tardigrada. Zoomorphology 127:21–36CrossRefGoogle Scholar
  251. Zhang Z-Q (2011) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148:1–237Google Scholar
  252. Zhang Z-Q (2013) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness (Addenda 2013). Zootaxa 3703:1–82PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Christine Martin
    • 1
  • Vladimir Gross
    • 1
  • Lars Hering
    • 1
  • Benjamin Tepper
    • 1
  • Henry Jahn
    • 1
  • Ivo de Sena Oliveira
    • 1
    • 2
  • Paul Anthony Stevenson
    • 3
  • Georg Mayer
    • 1
    Email author
  1. 1.Department of ZoologyUniversity of KasselKasselGermany
  2. 2.Departamento de Zoologia, Instituto de Ciências BiológicasUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  3. 3.Physiology of Animals and Behaviour, Institute of BiologyUniversity of LeipzigLeipzigGermany

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