Arthropod phylogeny: Onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage

Proceedings of the Royal Society B: Biological Sciences

Volumn 273, Issue 1596, 2006, Pages 1857-1866

  Strausfeld, Nicholas J ^a   Strausfeld, Camilla Mok ^a   Loesel, Rudi ^b   Rowell, David ^c   Stowe, Sally ^d  

^a UNIVERSITY OF ARIZONA   (United States)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Arthropod evolution; Brain organization; Chelicerata; Onychophora

Indexed keywords

ARACHNID; ARTHROPOD; BRAIN; EVOLUTION; PHYLOGENY; SPECIATION (BIOLOGY);

ARTHROPOD; ARTICLE; BRAIN REGION; CELL SHAPE; CLADISTICS; CONTROLLED STUDY; NERVE CELL; NEUROPIL; NONHUMAN; PARAPHYLY; PARSIMONY ANALYSIS; PHYLOGENY; PRIORITY JOURNAL; SILVER STAINING; SMELLING;

ARTHROPODA; CHELICERATA; EUPERIPATOIDES ROWELLI; HEXAPODA; MALACOSTRACA; MANDIBULATA; ONYCHOPHORA;

EID: 34250684507     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2006.3536     Document Type: Article

References (58)

1. Aguinaldo, A. M., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A. & Lake, J. A. 1997 Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489-493. (doi:10.1038/387489a0)
2. Ballard, J. W. O., Olsen, G. J., Faith, D. P., Odgers, W. A., Rowell, D. M. & Atkinson, P. W. 1992 Evidence from 125 ribosomal RNA sequences that onychophorans are modified arthropods. Science 258, 1345-1348.
3. Bartnik, E. & Weber, K. 1989 Widespread occurrence of intermediate filaments in invertebrates: common principles and aspects of diversion. Eur. J. Cell Biol. 50, 17-33.
4. Budd, G. E. 1996 The morphology of Opabinia regalis and the reconstruction of the arthropod stem group. Lethaia 29, 1-14.
5. Colgan, D. J., McLaughlan, A., Wilson, G. D. F., Livingston, S. P., Edgecomb, G. D., Macaranas, J., Cassis, G. & Gray, M. R. 1998 Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust. J. Zool. 46, 419-437. (doi:10.1071/ZO98048)
6. 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. Ann. Soc. Entomol. France 37, 85-103.
7. Duman-Scheel, M. & Patel, N. H. 1999 Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126, 2327-2334.
8. Edgecombe, G. D., Wilson, G. D. F., Colgan, D. J., Gray, M. R. & Cassis, G. 2000 Arthropod cladistics, combined analysis of histone H3 and U2 snRNA sequences and morphology. Cladistics 16, 155-203. (doi.10.1111/j.1096-0031.2000.tb00352.x)
9. Edgecombe, G. D., Giribet, G. & Wheeler, W. W. 2002 Phylogeny of Henicopidae (Chilopoda, Lithobiomorpha): a combined analysis of morphology and five molecular loci. Syst. Entomol. 27, 31-64. (doi:10.1046/j.0307-6970. 2001.00163.x)
10. Eriksson, B. J., Tait, N. N. & Budd, G. E. 2003 Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J. Morphol. 255, 1-23. (doi:10.1002/jmor.10034)
11. Fahrenbach, W. H. & Chamberlain, S. C. 1987 The brain of the horseshoe crab Limulus polyphemus. In Arthropod brain: its evolution, structure and functions (ed. A. P. Gupta), pp. 63-94. New York, NY: Wiley.
12. Fanenbruck, M. & Harzsch, S. 2005 A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct. Dev. 34, 343-378. (doi:10.1016/j.asd.2005.01.007)
13. Farris, S. M. 2005 Evolution of insect mushroom bodies: old clues, ne\v insights. Arthropod Struct. Dev. 34, 211-234. (doi:10.1016/j.asd. 2005.01.008)
14. Farris, S. M. & Sinakevitch, I. 2003 Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center. Arthropod Struct. Dev. 32, 79-101.
15. Flögel, J. H. L. 1876 Über den feineren Bau des Arthropodengehirns. Tagbl. Versamml. dtschr. Naturforsch. Ärzte. (Beilage) 49, 115-120.
16. Friedrich, M. & Tautz, D. 1995 Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of the myriapods. Nature 376, 165-167. (doi:10.1038/376165a0)
17. Giribet, G., Distel, D. L., Polz, M., Sterrer, W. & Wheeler, W. C. 2000 Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Syst. Biol. 49, 539-562. (doi:10.1080/10635159950127385)
18. Giribet, G., Edgecombe, G. & Wheeler, W. C. 2001 Arthropod phylogeny based on eight molecular loci and morphology. Nature 413, 157-161. (doi:10.1038/35093097)
19. Giribet, G., Edgecombe, G. D., Wheeler, W. W. & Babbit, C. 2002 Phylogeny and systematic position of Opiliones: a combined analysis of chelicerate relationships using morphological and molecular data. Cladistics 18, 5-70.
20. Grenier, J. K., Garber, T. L., Warren, R., Whitington, P. M. & Carroll, S. 1997 Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7, 547-553. (doi:10.1016/S0960-9822(06)00253-3)
21. Hanstrom, B. 1926 Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. (Facsimile reprint by A. Asher, Amsterdam 1968.)
22. Harzsch, S. 2003 Ontogeny of the ventral cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda. Arthropod Struct. Dev. 32, 17-38. (doi:10.1016/S1467-8039(03)00008-2)
23. Holmgren, N. 1916 Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden, und Insekten. K. Svenska Vetensk. Akad. Handl. 56, 1-200.
24. Hou, X. & Bergström, J. 1995 Cambrian lobopodians - ancestors of extant onychophorans? Zool. J. Linn. Soc. 114, 3-34. (doi:10.1006/zjls.1995.0014)
25. Immesberger, A. & Burmester, T. 2004 Putative phenoloxidases in the tunicate Ciona intestinalis and the origin of the arthropod hemocyanin superfamily. J. Comp. Physiol. B 174, 169-180. (doi:10.1007/s00360-003-0402-4)
26. Kenyon, F. C. 1896 The meaning and structure of the so-called "mushroom bodies" of the hexapod brain. Am. Nat. 30, 643-650. (doi:10.1086/276450)
27. Kusche, K., Ruhberg, H. & Burmeister, T. 2002 A hemocyanin from the Onychophora and the emergence of respiratory proteins. Proc. Natl Acad. Sci. USA 99, 10 545-10 548. (doi:10.1073/pnas.152241199)
28. Loesel, R., Nassel, D. R. & Strausfeld, N. J. 2002 Common design in a unique mid-line neuropil in the brains of arthropods. Arthropod Struct. Dev. 31, 77-91. (doi:10.1016/S1467-8039(02)00017-8)
29. McKinzie, M. E., Benton, J. L., Beltz, B. S. & 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. (doi:10.1002/cne.10716)
30. Mallatt, J. M., Garey, J. R. & Shultz, J. W. 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. (doi:10.1016/j.ympev.2003.07.013)
31. 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, 471-480. (doi:10.1016/j.asd.2005.03. 004)
32. Melzer, R. R., Michalke, M. & Smola, U. 2000 Walking on insect paths? Early ommatidial development in the compound eye of the ancestral crustacean, Triops cancriformis. Naturwissenschaften 87, 308-311. (doi:10.1007/s001140050727)
33. Michel, C. I., Kraft, R. & Restifo, L. L. 2004 Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24, 5798-5809. (doi:10.1523/JNEUROSCI.1102-04.2004)
34. 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. Genes Evol. 213, 9-17.
35. Orrhage, L. & Müller, M. C. M. 2005 Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia 535-536, 79-111.
36. Peterson, K. J. & Eernisse, D. J. 2001 Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences. Evol. Dev. 3, 170-205. (doi:10.1046/j.1525-142x.2001.003003170.x)
37. Popadic, A., Panganiban, G., Rusch, D., Shear, W. A. & Kaufman, T. C. 1998 Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev. Genes Evol. 208, 142-150. (doi:10.1007/s004270050165)
38. Ramsköld, L. & Chen, J. 1998 Cambrian lobopodians: morphology and phylogeny. In Arthropod fossils and phylogeny (ed. G. D. Edgecombe), pp. 107-150. New York, NY: Columbia University Press.
39. Regier, J. C., Shulz, J. W. & Kambic, R. E. 2005 Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc. R. Soc. B 272, 395-401. (doi:10.1098/rspb. 2004.2917)
40. Richter, S. 2002 The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Org. Divers. Evol. 2, 217-237. (doi:10.1078/1439-6092-00048)
41. Sandeman, D. & Scholtz, G. 1995 Ground plans, evolutionary changes and homologies in decapod crustacean brains. In The nervous system of invertebrates: an evolutionary and comparative approach (ed. O. Breidbach & W. Kutsch), pp. 329-347. Basel, Switzerland: Birkhauser.
42. Schürmann, F. W. 1987 Histology and ultrastructure of the onychophoran brain. In Arthropod brain: its evolution, structure and functions (ed. A. P. Gupta), pp. 159-180. New York, NY: Wiley.
43. Shaw, S. R. & Meinertzhagen, I. A. 1986 Evolutionary progression at synaptic connections made by identified homologous neurones. Proc. Natl Acad. Sci. USA 83, 7961-7965.
44. Sinakevitch, I., Douglass, J. K., Scholtz, G., Loesel, R. & Strausfeld, N. J. 2003 Conserved and convergent organisation in the optic lobes of insects and isopods, with reference to other crustacean taxa. J. Comp. Neurol. 467, 150-172. (doi:10.1002/cne.10925)
45. Strausfeld, N. J. 1998 Crustacean-insect relationships, the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav. Evol. 52, 186-206. (doi:10.1159/000006563)
46. Strausfeld, N. J. 2005 The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct. Dev. 34, 235-256. (doi:10.1016/j.asd.2005.04.001)
47. Strausfeld, N. J. & Barth, F. G. 1993 Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei. J. Comp. Neurol. 328, 43-62. (doi:10.1002/cne.903280104)
48. Strausfeld, N. J. & Li, Y. 1999 Representation of the calyces in the medial and vertical lobes of the cockroach mushroom bodies. J. Comp. Neurol. 409, 626-646. (doi:10.1002/(SICI)1096-9861(19990712)409: 4〈626::AID-CNE8〉 3.0.CO;2-B)
49. Strausfeld, N. J., Weltzien, P. & Barth, F. G. 1993 Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. J. Comp. Neurol. 328, 63-75. (doi:10.1002/cne.903280105)
50. Strausfeld, N. J., Buschbeck, E. K. & Gomez, R. S. 1995 The arthropod mushroom body, its roles, evolutionary enigmas and mistaken identities. In The nervous system of invertebrates, an evolutionary and comparative approach (ed. O. Breidbach & W. Kutsch), pp. 349-381. Basel, Switzerland: Birkhauser.
51. Strausfeld, N. J., Hansen, L., Li, Y.-S., Gomez, R. S. & Ito, K. 1998 Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem. 5, 11-37.
52. Stys, P. & Zrzavy, J. 1994 Phylogeny and classification of extant Arthropoda: review of hypotheses and nomenclature. Eur. J. Entomol. 91, 257-275.
53. Swofford, D. L. 2002 PAUP*: phylogenetic analysis using parsimony (*and other methods), v. 4.0.b10. Sunderland, MA: Sinauer Associates Inc.
54. Walossek, D. & Müller, K. J. 1998 Early arthropod phylogeny in the light of the Cambrian 'Orsten' fossils. In Arthropod fossils and phylogeny (ed. G. D. Edgecombe), pp. 185-231. New York, NY: Columbia University Press.
55. Waloszek, D., Chen, J., Maas, A. & Wang, X. 2005 Early Cambrian arthropods - new insights into arthropod head and structural evolution. Arthropod Struct. Dev. 34, 189-205. (doi:10.1016/j.asd.2005.01. 005)
56. Whitington, P. M. 2004 The development of the crustacean nervous system. In Evolutionary developmental biology of crustacea (ed. G. Scholtz). Crustacean issues, vol. 15, pp. 135-167. The Netherlands: A. A. Balkema.
57. Whitington, P. M., Meier, T. & King, P. 1991 Segmentation, neurogenesis and formation of early axonal pathways in the centipede, Erostigmus rubripes (Brandt). Wilhelm Roux's Arch. Dev. Biol. 199, 349-363.
58. Zrzavy, J., Mihulka, S., Kepka, P., Bezdek, A. & Tietz, D. 1998 Phylogeny of the metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14, 249-285. (doi:10.1111/j.1096-0031.1998.tb00338.x)