Abstract
Sipuncula is a small taxon of worm-like marine organisms of still uncertain phylogenetic position. Sipunculans are characterized by an unsegmented body composed of a trunk into which the anterior part, the introvert, can be withdrawn. The group has been placed at various positions within Metazoa; currently, it is either seen as sister group of a clade comprising Mollusca and Annelida or as sister to each of these. An in-group position in either Mollusca or Annelida has usually been precluded till now due to the lack of so-called annelid or molluscan “key-characters” such as segmentation and chaetae or the radula. In the development of certain taxa the trochophore stage is followed by a planktonic larva, the pelagosphera, which might exhibit phylogenetically important structures. Among these is the buccal organ, which has been considered homologous either to the ventral pharyngeal organ present in many sedentary polychaetes or to the radular apparatus of molluscs. In the present paper, the ventral pharynx of the pelagosphera larva of Phascolosoma agassizii is investigated by transmission electron microscopy. The pharynx comprises dorsolateral ciliary folds, a muscle bulb formed by transverse muscle fibres with large intercellular spaces, and an investing muscle. A tongue-like organ is lacking. These results show great structural correspondences to the ventral pharynx of polychaetes, especially to that of the flabelligerid Diplocirrus longisetosus. In contrast, there are no signs of structural similarities to the corresponding structures of molluscs. Thus evidence increases that Sipuncula are closely related to annelids; moreover, an in-group position of Sipuncula within Annelida, as suggested by recent molecular studies, is not precluded by the present data. Instead these studies find additional support. Hence the lack of segmentation and chitinous chaetae in Sipuncula would be a secondary rather than a primary situation, as has recently been shown for Echiura and Pogonophora.
Similar content being viewed by others
References
Adrianov AV, Malakhov VV, Maiorova AS (2005) Organization of the tentacle apparatus in a sipunculid Thysanocardia nigra Ikeda, 1904 (Sipuncula, Sipunculidea). Zool Zh 84:922–928 (in Russian)
Adrianov AV, Malakhov VV, Maiorova AS (2006) Postlarval ontogenesis of the tentacle apparatus in sipunculid Thysanocardia nigra Ikeda, 1904 (Sipuncula). Zool Zh 85 (in press) (in Russian)
Åkesson B (1958) A study of the nervous system of the Sipunculoideae with some remarks on the development of the two species Phascolion strombi Montagu and Golfingia minuta Keferstein. Unders Öresund 38:1–249
Ax P (1999) Das System der Metazoa II. Gustav Fischer, Stuttgart 1–383
Bleidorn C (2005) Phylogenetic relationships and evolution of Orbiniidae (Annelida, Polychaeta) based on molecular data. Zool J Linn Soc 144:59–73
Bleidorn C, Podsiadlowski L, Bartolomaeus T (2006) The complete mitochondrial genome of the orbiniid polychaete Orbinia latreillii (Annelida, Orbiniidae)—a novel gene order for Annelida and implications for annelid phylogeny. Gene. DOI 10.1016/j.gene.2005.11.018:1–8
Blumer MJF (1997) The larval ocelli of Golfingia misakiana (Sipuncula, Golfingiidae) and of a pelagosphera of another unidentified species. Zoomorphology 117:115–120
Boore JL, Staton JL (2002) The mitochondrial genome of the sipunculan Phascoliopsis gouldii supports its association with Annelida rather than Mollusca. Mol Bio Evol 19:127–137
Bunke D (1967) Zur Morphologie und Systematik der Aeolosomatidae Beddard 1895 and Potamodrilidae nov. fam. (Oligochaeta) Zool Jb Syst 94:187–368
Cutler EB (1994) The Sipuncula: their systematics, biology and evolution. Comstock Publ Ass, Ithaca, pp 1–453
Gerould JH (1906) The development of Phascolosoma. Studies on the embryology of the Sipunculidae I. Zool Jb Anat 23:77–162
Guralnick R (2002) A recapitulation of the rise and fall of the cell lineage research program: the evolutionary developmental relationship of cleavage to homology, body plans and life history. J Hist Biol 35:527–567
Guralnick R, Lindberg DR (2001) Reconnecting cell and animal lineages: what do cell lineages tell us about the evolution and development of Spiralia? Evolution 55:1501–1519
Filippova AV, Tzetlin AB, Purschke G (2003) Morphology and ultrastructure of the anterior end of Diplocirrus longisetosus Marenzeller, 1890 (Flabelligeridae, Polychaeta, Anneldia) Hydrobiologia 496:215–223
Halanych KM (2004) The new view of animal phylogeny. Annu Rev Ecol Evol Syst 35:229–256
Halanych KM, Dahlgren T, McHugh D (2002) Unsegmented annelids? Possible origin of four lophotrochozoan worm taxa. Integr Comp Biol 42:678–684
Haszprunar G (1996) The Mollusca: coelomate turbellarians or mesenchymate annelids? In: Taylor J (eds) Origin and evolution of the Mollusca. Oxford University, Oxford pp 3–28
Hausen H (2005) Comparative structure of the epidermis in polychaetes (Annelida). Hyobiologia 535/536:25–35
Hermans CO, Eakin RM (1969) Fine structure of the ocelli of a sipunculid, Phascolosoma agassizii. Z Zellforsch 100:325–339
Hermans CO, Eakin RM (1975) Sipunculan ocelli: fine structure in Phascolosoma agassizii. In: Rice ME, Todorovic M (eds) Proceedings of the international symposium on the biology of the Sipuncula and Echiura. Naucno Delo, Belgrade pp 229–237
Hessling R (2002) Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology 121:221–234
Hessling R (2003) Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia 496:225–239
Hessling R, Purschke G (2000) Immunohistochemical (cLSM) and ultrastructural analysis of the central nervous system and sense organs in Aeolosoma hemprichi (Annelida, Aeolosomatidae) Zoomorphology 120:65–78
Hessling R, Westheide W (2002) Are Echiura derived from a segmented ancestor?—immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol 252:100–113
Ivanov DL, Tzetlin AB (1981) Origin and evolution of the cuticular pharyngeal armature in trochophore animals having the ventral pharynx. Zool Zh 60: 1445–1454
Jägersten G (1963) On the morphology and behaviour of Pelagosphera larvae (Sipunculoidea). Zool Bidr Uppsala 25:551–570
Jouin C (1978) Anatomical and ultrastructural study of the pharyngeal bulb in Protodrilus (Polychaeta, Archiannelida). 2. The stomodeal epithelium and its cuticle. Tissue Cell 10:289–301
Kerth K (1983) Radulaapparat und Radulabildung der Mollusken. II. Zahnbildung, Abbau und Radulawachstum. Zool Jb Anat 110:239–269
Lundin K, Schander C (2003) Epidermal ciliary ultrastructure of adult and larval sipunculids (Sipunculida). Acta Zool (Stockh) 84:113–119
Mackenstedt U, Märkel K (1987) Experimental and comparative morphology of radula renewal in pulmonates (Mollusca, Gastropoda) Zoomorphology 107:209–239
Maxmen AB, King BF, Cutler EB, Giribet G (2003) Evolutionary relationships within the protostome phylum Sipuncula: a molecular analysis of ribosomal genes and histone H3 sequence data. Mol Phylogenet Evol 27:489–503
McHugh D (2005) Molecular systematics of polychaetes (Annelida). In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 535/536:309–318
Michel C (1978) Etude histologique, histochimique et cytologique du stomodeum chez le Polychète Sédentaire, Audouinia tentaculata (Montagu). Cah Biol Mar 19:433–446
Moritz K, Storch V (1970) Über den Aufbau des Integumentes der Priapuliden und Sipunculiden (Priapulus caudatus Lamarck, Phascolion strombi [Montagu]). Z Zellforsch 105:55–64
Nielsen C (2003) Proposing a solution to the Articulata-Ecdysozoa controversy. Zool Scr 32:475–482
Nielsen C, Scharff N, Eibye-Jacobsen D (1996) Cladistic analyses of the animal kingdom. Biol J Linn Soc Lond 57:385–410
Pilger JF (1982) Ultrastructure of the tentacles of Themiste lageniformuis (Sipuncula). Zoomorphology 100:143–156
Purschke G (1988a) Anatomy and ultrastructure of ventral pharyngeal organs and their phylogenetic importance in Polychaeta (Annelida). V. The pharynges of the Ctenodrilidae and Orbiniidae. Zoomoprhology 108:119–135
Purschke G (1988b) Pharynx. In: Westheide W, Hermans CO (eds) The ultrastructure of Polychaeta. Microfauna Mar 4:177–197
Purschke G (2002) On the ground pattern of Annelida. Org Divers Evol 2:181–196
Purschke G, Jouin C (1988) Anatomy and ultrastructure of the ventral pharyngeal organs of Saccocirrus (Saccocirridae) and Protodriloides (Protodriloidae fam. n.) with remarks on the phylogenetic relationships within the Protodrilida (Annelida: Polychaeta). J Zool Lond 215:405–432
Purschke G, Tzetlin AB (1996) Dorsolateral ciliary folds in the polychaete foregut: structure, prevalence and phylogenetic significance. Acta Zool (Stockh) 77:33–49
Purschke G, Wolfrath F, Westheide W (1997) Ultrastructure of the nuchal organ and cerebral organ in Onchnesoma squamatum (Sipuncula, Phascolionidae) Zoomorphology 117:23–31
Purschke G, Hessling R, Westheide W (2000) The phylogenetic position of the Clitellata and the Echiura—on the problematic assessment of absent characters. J Zool Syst Evol Res 38:165–173
Rice ME (1967) A comparative study of the development of Phascolosoma agassizii, Golfingia pugettensis, and Themiste pyroides with a discussion of developmental pattern in the Sipuncula. Ophelia 4:143–171
Rice ME (1973) Morphology, behavior, and histogenesis of the pelagosphera larva of Phascolosoma agassizii (Sipuncula). Smithson Contr Zool 132:1–51
Rice ME (1985) Sipuncula: developmental evidence for phylogenetic interference. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origin and relationships of lower invertebrates. Clarendon, Oxford pp 274–296
Rice ME (1993) Sipuncula. In: Harrison FW, Rice ME (eds) Microscopic anatomy of invertebrates, vol. 12. Onychophora, chilopoda and lesser protostomia. Wiley, New York pp 237–325
Robbins DE (1965) The biology and morphology of the pelagic annelid Poeobius meseres Heath. J Zool (Lond) 146:197–212
Rouse GW, Fauchald K (1995) The articulation of annelids. Zool Scr 24:269–301
Rouse GW, Pleijel F (2001) Polychaetes. Oxford University, Oxford pp 1–354
Ruppert EE, Rice ME (1983) Structure, ultrastructure, and function of the terminal organ of a pelagosphera larva (Sipuncula). Zoomorphology 102:143–163
Scheltema AH (1993) Aplacophora as progenetic aculiferans and the coelomate origin of mollusks as the sister taxon of Sipuncula. Biol Bull 184:57–78
Scheltema AH (1996) Phylogenetic position of Sipuncula, Mollusca and the progenetic Aplacophora. In: Taylor J (eds) Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford pp 53–58
Schulze A, Cutler EB, Giribet G (2005) Reconstructing the phylogeny of the Sipuncula. In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 535/536:275–294
Todt C, Salvini-Plawen Lv (2004) Ultrastructure and histochemistry of the foregut in Wirenia argentea and Genitoconia rosea (Mollusca, Solenogastres). Zoomorphology 123:65–80
Todt C, Salvini-Plawen Lv (2005) The digestive tract of Helicoradomenia (Solenogastres, Mollusca), aplacophoran molluscs from the hydrothermal vents on the East Pacific Rise. Inv Biol 124:230–253
Tzetlin AB (1987) Fine morphology of the pharynx apparatus in the larvae of Nicolea zostericola (Polychaeta Terebellidae). Dokl Akad NAUK SSSR 293:1505–1509
Tzetlin AB (1991) Evolution of the feeding apparatus in the polychaetes of the order Capitellida. Zool Zh 70:757–760 (in Russian)
Tzetlin A, Purschke G (2005) Pharynx and intestine. In: Bartolomaeus T, Purschke G (eds) Morphology, molecules, evolution and phylogeny in Polychaeta and related taxa. Hydrobiologia 535/536:199–225
Valembois P, Boiledeu D (1980) Fine structure and functions of haemerythrocytes and leucocytes of Sipunculus nudus. J Morphol 163:69–77
Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM (2005) Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol 215:509–518
Zrzavý J, Mihulka S, Kepka P, Bezděk A, Tietz D (1998) Phylogeny of the Metazoa based on morphological and 18S ribosomal DNA evidence. Cladistics 14:249–285
Acknowledgments
We gratefully acknowledge the help of our colleague Ed Ruppert in making available the embedded material for this investigation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tzetlin, A.B., Purschke, G. Fine structure of the pharyngeal apparatus of the pelagosphera larva in Phascolosoma agassizii (Sipuncula) and its phylogenetic significance. Zoomorphology 125, 109–117 (2006). https://doi.org/10.1007/s00435-006-0025-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-006-0025-x