Zoomorphology

, Volume 115, Issue 3, pp 161–177

Structure and formation of the uncini in Pectinaria koreni, Pectinaria auricoma (Terebellida) and Spirorbis spirorbis (Sabellida): inplications for annelid phylogeny and the position of the Pogonophora

  • Thomas Bartolomaeus
Original Article

Abstract

Setation is an important taxonomic character of the Annelida. Within this taxon, Terebellida and Sabellida both have transverse rows of short, apically toothed setae which are situated inside the neuropodial rim. The apical spines are curved and their tips point anteriorly. These setae are termed uncini. In the terebellidans Pectinaria koreni, Pectinaria auricoma and in the sabellidan Spirorbis spirorbis, these setae arise from a follicle which consists of a chaetoblast and two follicle cells. The special structure of the uncini is a result of temporal modifications of the actin-filament system of the chaetoblast and changing spatial interactions between the chaetoblast and the follicle cells during the formation of these setae. Once the uncinus is formed, the microvilli are withdrawn and electron-dense material is deposited in the remaining canals. The microvilli are replaced by short processes of the chaetoblast, and the actin-filament system is replaced by a system of intermediate filaments which help to mechanically attach the uncinus to the follicle. Such uncini are also described in both pogonophoran groups, the Perviata and the Obturata (Vestimentifera). In several structural details they correspond to those of the species investigated in this paper, so that the hypothesis of a homology of the uncini seems to be justified. This hypothesis leads to the conclusion that uncini evolved in the common stem lineage of Pogonophora, Terebellida and Sabellida, implying a monophyletic origin of these three taxa. The uncini are compared to the hooked setae of the Arenicolida, Maldanida and Psammodrilida, which are also aligned in transverse rows inside the neurophodial rim. Hooked setae and uncini are hypothesized to be homologous. It, therefore, can be concluded that Arenicolida, Maldanida and Psammodrilida are closely related to the monophylum consisting of Terebellida, Sabellida and Pogonophora, and that these six taxa share a common ancestor, which evolved transverse rows of setae with apically curved spines and a formative site lateral to the edge of the neuropodial rim. According to the phylogenetic relationships proposed here, the Pogonophora are a subordinate taxon within the Annelida.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ashworth JH (1912) Catalogue of the Chaetopoda in the British Museum (Natural History). A. Polychaeta (1). Arenicolidae. British Museum, LondonGoogle Scholar
  2. Bartolomaeus T (1994a) On the coelomic lining of the Annelida, Echiura and Sipuncula. Microfauna Mar 9:171–220Google Scholar
  3. Bartolomaeus T (1994b) Ultrastruktur und Entwicklung der Uncini und deren Bedeutung für die Systematik der Anneliden. Verh Dtsch Zool Ges 87(1):215Google Scholar
  4. Bartolomaeus T (1995) Ultrastructure of the protonephridia in larval Magelona mirabilis (Spionida) and Pectinaria auricoma (Terebellida): Head kindeys in the ground pattern of the Annelida. Microfauna Mar 10 (in press)Google Scholar
  5. Bobin G (1944) Morphogénèse des soies chez les Annélides Polychètes. Ann Inst Ocean 22:1–106Google Scholar
  6. Bookhout CG, Horn EC (1949) The development of Axiothella mucosa (Andrews). J Morphol 84:145–173Google Scholar
  7. Bouligand Y (1967) Les soies et les cellules associées chez deux Annélides Polychètes. Étude en microscopie photonique à contraste de phase et en microscopie électronique. Z Zellforsch Mikrosk Anat 79:332–363Google Scholar
  8. Brocco SL, O'Clair RM, Cloney RA (1974) Cephalopod integument: The ultrastructure of Kölliker's organs and their relationship to setae. Cell Tissue Res 151:293–308Google Scholar
  9. Doyle S (1991) Setal type and distribution in Australian species of Scyphoproctus (Polychaeta, Capitellidae) and three other capitellids, with a description of Scyphoproctus towraiensís sp.n. Zool Scr 20:263–275Google Scholar
  10. Fauchald K (1977) The polychaete worms. Definitions and keys to the orders, families and genera. Nat Hist Mus Los Angeles Sci Series 28:1–188Google Scholar
  11. Flügel H-J, Callsen-Cencic P (1994) Über die systematische Stellung der Pogonophora und Vestimentifera. Verh Dtsch Zool Ges 87(1):221Google Scholar
  12. Gamble FW, Ashworth JH (1900) The anatomy and classification of the Arenicolidae, with some observations on their post-larval stages. Q J Microsc Sci 43:419–569Google Scholar
  13. Gardiner SL (1992) Polychaeta: General organization, integument, musculature, coelom, and vascular system. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates 7: Annelida. Wiley-Liss, New York, pp 19–52Google Scholar
  14. Gardiner SL, Jones ML (1993) Vestimentifera. In: Harrison FW, Rice ME (eds) Microscopic anatomy of invertebrates 12: Onychophora, Chilopoda and lesser Protostomata. Wiley-Liss, New York, pp 371–460Google Scholar
  15. Gardiner SL, Jones ML (1994) On the significance of larval and juvenile morphology for suggesting phylogenetic relationships of the Vestimentifera. Am Zool 34:513–522Google Scholar
  16. George JD, Hartmann-Schröder G (1985) Polychaetes: British Amphinomida, Sphintherida and Eunicida. In: Kermack DM, Barnes RSK (eds) Synopses of the British fauna 32. Brill and Backhuys, London, pp 1–221Google Scholar
  17. George DJ, Southward EC (1973) A comparative study of the setae of Pogonophora and polychaetous Annelida. J Mar Biol Assoc UK 53:403–424Google Scholar
  18. Gupta BL, Little C (1970) Studies on Pogonophora. 4. Fine structure of the cuticle and epidermis. Tissue Cell 2:637–696Google Scholar
  19. Hartman O (1954) Pogonophora Johansson, 1938. Syst Zool 3:183–185Google Scholar
  20. Hartmann-Schröder G (1971) Annelida, Borstenwürmer, Polychaeta. In: Dahl M, Peus F (eds) Tierwelt Deutschlands 58. G. Fischer, Jena, pp 1–594Google Scholar
  21. Holthe T (1986) Evolution, systematics, and distribution of the Polychaeta Terebellomorpha, with a catalogue of the taxa and a bibliography. Gunneria 55:1–236Google Scholar
  22. Jägersten G (1956) On the larva of Siboglinum ekmani sp.n., encountered in Skagerak with some general remarks on the group Pogonophora. Zool Bidr Uppsala 31:211–252Google Scholar
  23. Jones ML (1985) Vestimentiferan pogonophores: their biology and affinities. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. Synstematics Association, spec. vol 28. Clarendon Press, Oxford, pp 327–342Google Scholar
  24. Jones ML, Gardiner SL (1988) Evidence for a transient digestive tract in Vestimentifera. Proc Biol Sco Wash 101:423–433Google Scholar
  25. Jones Ml, Gardiner SL (1989) On the early development of the vestimentiferan tube worm Ridgeia sp. and observations on the nervous system and the trophosome in Ridgeia sp. and Riftia pachyptila. Biol Bull (Woods Hole) 177:254–276Google Scholar
  26. Knight-Jones P (1981) Behaviour, setal inversion and phylogeny of Sabellida (Polychaeta). Zool Scr 10:183–202Google Scholar
  27. Knight-Jones P, Fordy MR (1979) Setal structure, functions and interrelationships in Spirorbidae (Polychaeta, Sedentaria). Zool Scr 8:119–138Google Scholar
  28. Kristensen RM, Nørrevang A (1982) Description of Psammodrilus aedificator sp.n. (Polychaeta), with notes on the arctic interstitial fauna of Disko Island, W. Greenland. Zool Scr 11:265–279Google Scholar
  29. Land J van der, Nørrevang A (1975) The systematic position of Lamellibrachia (Annelida, Vestimentifera). In: Norrevang A (ed) The phylogeny and systematic position of Pogonophora, proceedings of a symposium held at the Zoological Central Institute, University of Copenhagen November 1973. Z Zool Syst Evolutionsforsch (Suppl):86:101Google Scholar
  30. Nielsen C (1987) Structure and function of metazoan ciliary bands and their phylogenetic significance. Acta Zool 68:205–262Google Scholar
  31. Nielsen C (1995) Animal Evolution. Interrelationships of living phyla. Oxford University Press, OxfordGoogle Scholar
  32. Nilsen R, Holthe T (1985) Arctic and scandinavian Oweniidae (Polychaeta) with a description of Myriochele fragilis sp.n., and comments on the phylogeny of the family. Sarsia 70:17–32Google Scholar
  33. O'Clair RM, Cloney RA (1974) Patterns of morphogenesis mediated by dynamic microvilli: Chaetogenesis in Nereis vexillosa. Cell Tissue Res 151:141–157Google Scholar
  34. Orrhage L (1973) Light and electron microscopic studies of some brachiopod and pogonophoran setae. Z Morphol Tiere 74:253–270Google Scholar
  35. Pettibone M (1982) Annelida: Polychaeta. In: Parker SP (ed) Synopsis and classification of living organisms 2. McGraw-Hill, New York, pp 3–43Google Scholar
  36. Rosenfeld P (1982) Zur Ultrastruktur und taxonomischen Bedeutung der Borsten (Setae) und Haken (Uncini) von Polychaeten. Zool Jb Syst 109:268–289Google Scholar
  37. Southward EC (1988) Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): Implications for relationship between Vestimentifera and Pogonophora. J Mar Biol Assoc UK 62:889–906Google Scholar
  38. Southward EC (1993) Pogonophora. In: Harrison FW, Rice ME (eds) Microscopic anatomy of invertebrates 12: Onychophora, Chilopoda, and lesser Protostomata. Wiley-Liss, New York, pp 327–369Google Scholar
  39. Specht A (1988) Chaetae. In: Westheide W, Hermans CO (eds) The ultrastructure of the Polychaeta. Microfauna Mar 4:45–59Google Scholar
  40. Storch V (1984) Echiura and Sipuncula. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument 1. Springer, Berlin, pp 368–375Google Scholar
  41. Storch V, Welsch U (1972) Über Bau und Entstehung der Mantelrandstacheln von Lingula unguis L. (Brachiopoda). Z Wiss Zool 183:181–189Google Scholar
  42. Swedmark B (1955) Recherches sur la morphologie, de dévelopement et la biologie de Psammodrilus balanoglossoides Polychaete sédentaire de la microfaune des sables. Arch Zool Exp Gen 92:141–220Google Scholar
  43. Swedmark B (1958) Psammodriloides fauveli n. gen., n. sp. et la famille des Psammodrilidae (Polychaeta Sedentaria). Ark Zool 12:55–64Google Scholar
  44. Thomassin BA, Picard C (1972) Étude de la microstructure des soies de polychètes Capitellidae et Oweniidae au microscope électronique à balayage: un critère systématique précis. Mar Biol 12:229–236Google Scholar
  45. Wells GP (1959) The genera of the Arenicolidae (Polychaeta). Proc Zool Soc London 133:301–314Google Scholar
  46. Westheide W, Watson Russel C (1992) Ultrastructure of chrysopetalid paleal chaetae (Annelida, Polychaeta). Acta Zool 73:197–202Google Scholar
  47. Williams NA, Dixon DR, Southward EC, Holland PWH (1993) Molecular evolution and diversification of the vestimentiferan tube worm. J Mar Biol Assoc UK 73:437–452Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • Thomas Bartolomaeus
    • 1
  1. 1.II. Zoologisches Institut und MuseumGöttingenGermany

Personalised recommendations