Abstract
Comparative morphology currently permits no unambiguous decision on the primary homology of the nephridia of Annelida and Arthropoda. In order to obtain additional information on this subject, ultrastructure of morphogenesis and further differentiation of nephridia was studied in the onychophoran Epiperipatus biolleyi (Peripatidae). In this species, the nephridial anlage develops by reorganization of the lateral portion of the embryonic coelomic wall that initially gives rise to a ciliated canal. All other structural components, including the sacculus, merge after the nephridial anlage has been separated from the remaining mesodermal tissue. The nephridial sacculus does not represent a ‘persisting coelomic cavity’, since it arises de novo during embryogenesis. There is no evidence for ‘nephridioblast‘ cells participating in the nephridiogenesis of Onychophora, which is in contrast to the general mode of nephridial formation in Annelida. Available data on nephridiogenesis in euarthropods (Chelicerata, Myriapoda, Crustacea, and Hexapoda) also provide no evidence for nephridia of Annelida and Arthropoda being a synapomorphy of these taxa. These findings accordingly weaken the traditional Articulata hypothesis.
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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
Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford
Ax P (1996) Multicellular animals. A new approach to the phylogenetic order in nature, vol 1. Springer, Berlin Heidelberg New York
Ax P (2000) Multicellular animals. The phylogenetic system of the metazoa, vol 2. Springer, Berlin Heidelberg New York
Bahl KN (1922) On the development of the ‘enteronephric’ type of nephridial system in earthworms of the genus Pheretima. Q J Microsc Sci 68:67–99
Balavoine G, Adoutte A (2003) The segmented Urbilateria: a testable scenario. Integr Comp Biol 43:137–147
Bartolomaeus T (1989) Ultrastructure and development of the nephridia in Anaitides mucosa (Annelida, Polychaeta). Zoomorphology 109:15–32
Bartolomaeus T (1997) Structure and development of the nephridia of Tomopteris helgolandica (Annelida). Zoomorphology 117:1–11
Bartolomaeus T (1999) Structure, function and development of segmental organs in Annelida. Hydrobiologia 402:21–37
Bartolomaeus T, Ax P (1992) Protonephridia and metanephridia - their relation within the Bilateria. Z zool Syst Evolutionsforsch 30:21–45
Bartolomaeus T, Quast B (2005) Structure and development of nephridia in Annelida and related taxa. Hydrobiologia 535/536:139–164
Bartolomaeus T, Ruhberg H (1999) Ultrastructure of the body cavity lining in embryos of Epiperipatus biolleyi (Onychophora, Peripatidae) - a comparison with annelid larvae. Invertebr Biol 118:165–174
Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Anat 86:307–458
Bergh RS (1898) Nochmals über die Entwicklung der Segmentalorgane. Z wiss Zool 66:435–449
Boore JL, Brown WM (2000) Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol 17:87–106
Brauer A (1895) Beiträge zur Kenntnis der Entwicklungsgeschichte des Skorpions. II. Z wiss Zool 59:351–433
Brusca C, Brusca GJ (2003) Invertebrates, 2nd edn. Sinauer Association, Sunderland
Budd G (2001) Why are arthropods segmented? Evol Dev 3:332–342
Bunke D (2003) Early development of metanephridia in the caudal budding zone of a clitellate annelid, Dero digitata (Naidida): an electron-microscopical study. Acta Zool 84:87–97
Buxton BH (1917) Notes on the anatomy of arachnids. The coxal glands of the arachnids. The ganglia of the arachnids. J Morphol 29:1–25
Dohle W (1979) Vergleichende Entwicklungsgeschichte des Mesoderms bei Articulaten. In: Siewing R (ed) Ontogenese und Phylogenese - Erlanger Symposium für Strukturanalyse und Evolutionsforschung, 3.-6. Oktober 1977, Fortschritte in der Zoologischen Systematik und Evolutionsforschung. Paul Parey, Hamburg, pp 120–140
Dohle W (1980) Sind die Myriapoden eine monophyletische Gruppe? Abh Naturwiss Ver Hamburg 23:45–104
Dohle W (1996) Antennata (Tracheata, Monoantennata, Atelocerata). In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp 582–600
Dove H, Stollewerk A (2003) Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development 130:2161–71
Dunger W (1993) Überklasse Antennata. In: Gruner H-E (ed) Lehrbuch der Speziellen Zoologie, Band I: Wirbellose Tiere. 4.Teil: Arthropoda (ohne Insecta). Gustav Fischer, Stuttgart, pp 1031–1159
Evans R (1901) On the Malayan species of Onychophora. Part II. - The development of Eoperipatus weldoni. Q J Microsc Sci 45:41–88
Feustel H (1958) Untersuchungen über die Exkretion bei Collembolen (Ein Beitrag zur Exkretion bei Arthropoden). Z wiss Zool 161:209–238
François J (1969) Anatomie et morphologie céphalique des Protoures (Insecta Apterigota). Mém Mus Nat Hist Nat Paris 49:1–144
François J, Dallai R (1986) Ultrastructure des glandes maxillaires d′Acerentomon affine Bagn. et d′Eosentomon transitorium Berl. (Apterygota: Protura). Int J Insect Morphol Embr 15:201–212
Friedrich M, Tautz D (1995) Ribosomal DNA phylogeny of the major extant arthropod classes and the evolution of myriapods. Nature 376:165–167
Giribet G (2003) Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology 106:303–326
Giribet G, Richter S, Edgecombe GD, Wheeler WC (2005) The position of crustaceans within the arthropoda—evidence from nine molecular loci and morphology. In: Koenemann S, Jenner RA (eds) Crustacea and Arthropod relationships. CRC Press, Boca Raton, pp 307–352
Glen EH (1918) A revision of certain points in the early development of Peripatus capensis. Q J Microsc Sci 63:283–292
Goodrich ES (1895) On the coelom, genital ducts, and nephridia. Q J Microsc Sci 37:477–508
Goodrich ES (1932) On the nephridiostome of Lumbricus. Q J Microsc Sci 75:165–179
Goodrich ES (1945) The study of nephridia and genital ducts since 1895. Q J Microsc Sci 86:113–392
Haase A, Stern M, Wächtler K, Bicker G (2001) A tissue-specific marker of Ecdysozoa. Dev Genes Evol 211:428–433
Harzsch S (2004) Phylogenetic comparison of serotonin-immunoreactive neurons in representatives of the Chilopoda, Diplopoda, and Chelicerata: implications for arthropod relationships. J Morphol 259:198–213
Harzsch S, Müller CHG, Wolf H (2005) From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sistergroup relationship of Chelicerata and “Myriapoda” but favour the Mandibulata concept. Dev Genes Evol 215:53–68
Haupt J (1969) Zur Feinstruktur der Labialniere des Silberfischchens Lepisma saccharina L. (Thysanura, Insecta). Zool Beitr 15:139–170
Hessler RR, Elofsson R (1991) The excretory system of Hutchinsoniella macracantha (Crustacea: Cephalocarida). J Crust Biol 11:356–367
Heymons R (1901) Die Entwicklungsgeschichte der Scolopender. Zoologica 33:1–244
Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157
Jenner RA, Scholtz G (2005) Playing another round of metazoan phylogenetics: Historical epistemology, sensitivity analysis, and the position of Arthropoda within the Metazoa on the basis of morphology. In: Koenemann S, Jenner RA (eds) Crustacea and Arthropod relationships. CRC Press, Boca Raton, pp 355–385
Johannsen O, Butt FH (1941) Embryology of insects and myriapods. McGraw-Hill Book Company, New York
Kadner D, Stollewerk A (2004) Neurogenesis in the chilopod Lithobius forficatus suggests more similarities to chelicerates that to insects. Dev Genes Evol 214:367–79
Kennel J von (1888) Entwicklungsgeschichte von Peripatus edwardsii Blanch. und Peripatus torquatus n.sp. II. Theil. Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg 8:1–93
Kingsley JS (1885) Notes on the embryology of Limulus. Q J Microsc Sci 25:521–576
Kingsley JS (1893) The embryology of Limulus—Part II. J Morphol 8:195–268
Kitamura K, Shimizu T (2000a) Embryonic expression of alkaline phosphatase activity in the oligochaete annelid Tubifex. Invertebr Reprod Dev 37:69–73
Kitamura K, Shimizu T (2000b) Analyses of segment specific expression of alkaline phosphatase activity in the mesoderm of the oligochaete annelid Tubifex: implication for specification of segmental identity. Dev Biol 219:214–223
Klausnitzer B (1996) Insecta (Hexapoda), Insekten. In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp 601–681
Lavallard R, Campiglia S (1983) Sur la ciliature des nephridies chez Peripatus acacioi Marcus et Marcus (Onychophora: Peripatidae). Arch d’Anat Microsc Morphol Exp 72:183–197
Lebedinsky J (1892) Die Entwicklung der Coxaldrüsen bei Phalangium. Zool Anz 15:131–137
Lillie RS (1905) The structure and development of the nephridia of Arenicola cristata Stimpson. Mitt Zool Neapel 17:341–405
Mallatt J, Winchell CJ (2002) Testing the new animal phylogeny: first use of combined large-subunit and small-subunit rRNA gene sequences to classify the protostomes. Mol Biol Evol 19:289–301
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 Phyl Evol 31:178–191
Manton SM (1928) On the embryology of a mysid crustacean, Hemimysis lamornae. Philos Trans R Soc Lond B Biol Sci 216:363–463
Manton SM (1934) On the embryology of the crustacean Nebalia bipes. Philos Trans R Soc Lond B Biol Sci 223:163–238
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. Arthr Str Dev (in press)
Mayer G, Ruhberg H, Bartolomaeus T (2004) When an epithelium ceases to exist—An ultrastructural study on the fate of the embryonic coelom in Epiperipatus biolleyi (Onychophora, Peripatidae). Acta Zool 85:163–170
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 263:60–70
Meyer A (1929) Die Entwicklung der Nephridien und Gonoblasten bei Tubifex rivulorum Lam. - nebst Bemerkungen zum natürlichen System der Oligochaeten. Z wiss Zool 98:135–178
Moritz M (1959) Zur Embryonalentwicklung der Phalangiiden (Opiliones; Palpatores) II. Die Anlage und Entwicklung der Coxaldrüse bei Phalangium opilio L. Zool Jb Anat 77:229–240
Nielsen C (1997) The phylogenetic position of the Arthropoda. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 11–22
Nielsen C (2001) Animal evolution: Interrelationships of the Living Phyla. Oxford University Press, Oxford
Okada K (1988) Annelida. In: Kumé M, Dan K (eds) Invertebrate embryology. reprinted by Garland Publishing, New York, pp 192–241
Patten WM, Hazen AP (1900) The development of the coxal gland, branchial cartilages, and genital ducts of Limulus polyphemus. J Morphol 16:459–502
Penners A (1923) Die Entwicklung des Keimstreifs und die Organbildung bei Tubifex rivulorum Lam. Zool Jb Anat 45:251–308
Pflugfelder O (1948) Entwicklung von Paraperipatus amboinensis n. sp. Zool Jb Anat 69:443–492
Pflugfelder O (1980) Onychophora. In: Seidel F (ed) Morphogenese der Tiere, 1. Reihe, Lieferung 4. Gustav Fischer, Jena, pp 13–76
Philippe H, Lartillot N, Brinkmann H (2005) Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol Biol Evol 22:1246–1253
Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136
Rouse GW, Fauchald K (1995) The articulation of annelids. Zool Scr 24:269–301
Rouse G, Fauchald K (1997) Cladistics and polychaetes. Zool Scr 26:139–204
Ruppert EE, Smith PR (1988) The functional organisation of filtration nephridia. Biol Rev 63:231–258
Ruppert EE, Fox RS, Barnes RD (2004) Invertebrate biology, 7th edn. Thomson Brooks/Cole, Belmont
Schaefer K, Haszprunar G (1997) Anatomy of Laevipilina antarctica, a monoplacophoran limpet (Mollusca) from Antarctic waters. Acta Zool 77:295–314
Schmidt-Rhaesa A (2003) Old trees, new trees – is there any progress? Zoology 106:291–301
Schmidt-Rhaesa A (2004) Ecdysozoa versus Articulata. In: Richter S, Sudhaus W (eds) Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin. Goecke & Evers, Keltern, pp 35–49
Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR (1998) The position of the Arthropoda in the phylogenetic system. J Morphol 238:263–285
Schminke HK (1996) Crustacea, Krebse. In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp 501–581
Scholl G (1963) Embryologische Untersuchungen an Tanaidaceen (Heterotanais oerstedi Kröyer). Zool Jb Anat 80:500–554
Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154
Scholtz G (1997) Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey RA, Thomas RH (eds) Arthropod Relationships, vol. 24. Chapman & Hall, London, pp 317–332
Scholtz G (2002) The Articulata hypothesis - or what is a segment? Org Divers Evol 2:197–215
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, Moscow, pp 489–501
Seaver, EC (2003) Segmentation: mono- or polyphyletic? Int J Dev Biol 47:583–595
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 27:467–550
Sedgwick A (1888) The development of the Cape species of Peripatus. Part IV. The changes from stage G to birth. Q J Microsc Sci 28:373–396
Seifert G (1979) Considerations about the evolution of excretory organs in terrestrial arthropods. In: Camatini M (ed) Myriapod biology. Academic, London, pp 353–372
Sekiguchi K (1988) Arthropoda. II. Arachnida. In: Kumé M, Dan K (eds) Invertebrate Embryology. Reprinted by Garland Publishing, New York, pp 389–404
Sheldon L (1887) On the development of Peripatus novae-zealandiae. Q J Microsc Sci 28:205–237
Shiino SM (1988) Arthropoda. I. Crustacea. In: Kumé M, Dan K (eds) Invertebrate Embryology. Reprinted by Garland Publishing, New York, pp 333–388
Shimizu T, Nakamoto A (2001) Segmentation in annelids: cellular and molecular basis for metameric body plan. Zool Sci 18:285–298
Shimizu T, Kitamura K, Arai A, Nakamoto A (2001) Pattern of formation in embryos of the oligochaete annelid Tubifex: cellular basis for segmentation and specification of segmental identity. Hydrobiologia 463:123–131
Siewing R (1953) Morphologische Untersuchungen an Tanaidaceen und Lophogastriden. Z wiss Zool 157:333–426
Smith PR, Ruppert EE (1988) Nephridia. Micr Mar 4:231–262
Staff F (1910) Organogenetische Untersuchungen über Criodrilus lacuum. Arbeiten aus dem Zoologischen Institut der Universität Wien 18:227–256
Storch V, Ruhberg H (1993) Onychophora. In: Harrison FW, Rice ME (eds) Microscopic Anatomy of Invertebrates, vol 12. Wiley-Liss, New York, pp 11–56
Storch V, Ruhberg H, Alberti G (1978) Zur Ultrastruktur der Segmentalorgane der Peripatopsidae (Onychophora). Zool Jb Anat 100:47–63
Sudhaus W, Rehfeld K (1992) Einführung in die Phylogenetik und Systematik. Gustav Fischer, Stuttgart
Tiegs OW (1940) The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q J Microsc Sci 82:1–225
Tiegs OW (1947) The development and affinities of the Pauropoda, based on a study of Pauropus silvaticus. Part I. Q J Microsc Sci 88:165–267
Vanderbroek G (1935) Organogénèse du système néphridien chez les oligochètes et plus spécialement chez Eisenia foetida Sav. Rec Inst Zool Torley-Rousseau 5:5–72
Vejdovsky F (1892) Entwicklungsgeschichtliche Untersuchungen (Heft III). Die Organogenie der Oligochaeten. J. Otto, Prag, pp 299–360
Wägele J-W (2005) Foundations of Phylogenetic Systematics. Dr Friedrich Pfeil, München
Wägele J-W, Misof B (2001) On quality of evidence in phylogeny reconstruction: a reply to Zrzavý’s defence of the “Ecdysozoa” hypothesis. J Zool Syst Evol Res 39:165–176
Wägele J-W, Erikson T, Lockhart P, Misof B (1999) The Ecdysozoa: artifact or monophylum? J Zool Syst Evol Res 37:211–223
Weygoldt P (1958) Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex (L). Zool Jb Anat 77:51–110
Weygoldt P (1964) Vergleichend-embryologische Untersuchungen an Pseudoscorpionen (Chelonethi). Z Morphol Ökol Tiere 54:1–106
Weygoldt P (1965) Vergleichend-embryologische Untersuchungen an Pseudoscorpionen. III. Die Entwicklung von Neobisium muscorum Leach (Neobisiinae, Neobisiidae). Mit dem Versuch einer Deutung der Evolution des embryonalen Pumporgans. Z Morphol Ökol Tiere 55:321–382
Weygoldt P (1986) Arthropod interrelationships: The phylogenetic-systematic approach. Z zool Syst Evolutionsforsch 24:19–35
Weygoldt P (1996) Chelicerata, Spinnentiere. In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp 449–497
Wiesenmüller B, Rothe H, Henke W (2003) Phylogenetische systematik. Springer, Berlin Heidelberg New York
With C (1904) The Notostigmata, a new suborder of Acari. Vidensk Medd Naturh Foren København 1904:137–192
Woodring JP (1973) Comparative morphology, functions, and homologies of the coxal glands in oribatid mites (Arachnida: Acari). J Morphol 139: 407–429
Yoshikura M (1955) Embryological studies on the liphistiid spider Heptathela kumurai. II. Kumamoto J Sci B2:1–86
Acknowledgements
My sincere thanks are expressed to the staff of the Instituto Nacional de Biodiversidad (INBio) in Costa Rica, especially to Alvaro Herrera, for collecting the animals, dissecting, fixing, and sending the material to me. I thank Thomas Bartolomaeus, Gregory Edgecombe, Markus Koch, Hilke Ruhberg and Gerhard Scholtz for giving some critical comments and useful suggestions on the manuscript. Ira Richling kindly helped to get contact to the staff of the INBio. I am thankful to Björn Quast for writing software for a more comfortable handling of the electron microscopic data. This study was supported by the Studienstiftung des deutschen Volkes (D/2002 0033) and the Deutsche Forschungsgemeinschaft (BA 1520/8-1, 8-2; RU 358/4-1, 4-2).
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Mayer, G. Origin and differentiation of nephridia in the Onychophora provide no support for the Articulata. Zoomorphology 125, 1–12 (2006). https://doi.org/10.1007/s00435-005-0006-5
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DOI: https://doi.org/10.1007/s00435-005-0006-5