Abstract
Spermiogenesis in the polychaete species Diurodrilus subterraneus may be divided into six stages. These stages, as well as the ultrastructure of the mature spermatozoa, are described based on TEM studies. The spermatozoa are unusual in having a very large acrosome followed by a region containing the nucleus and several ovoid mitochondria. A secondary acrosomal membrane forms a manchette around the nucleus and mitochondria. In this region, the plasma membrane is modified, with many small, mushroom-shaped cytoplasmic processes, each including filaments. The flagellum may be divided into three sequential regions; the longest, middle one is covered by a helically arranged mucous coat. Spermatozoa of the type described here are unknown among polychaetes but show certain superficial resemblances to those in oligochaetes. The resemblance of the mushroom-shaped bodies to spermatozoal microvilli in certain gnathostomulids is discussed. The phylogenetic relationships of Diurodrilidae are considered on the basis of this new information.
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References
Afzelius BA, Franzén Å (1971) The spermatozoon of the jellyfish Nausithoe. J Ultrastruct Res 37:186–199
Ax P (1956) Die Gnathostomulida, eine rätselhafte Wurmgruppe aus dem Meeressand. Abh Math Naturwiss Kl Akad Wiss Mainz, Jahrg 1956 (8):1–32
Ax P (1967) Diurodrilus ankeli nov. spec. (Archiannelida) von der nordamerikanischen Pazifikküste. Ein Beitrag zur Morphologie, Systematik und Verbreitung der Gattung Diurodrilus. Z Morphol Ökol Tiere 60:5–16
Ax P (1985) The position of the Gnathostomulida and Platyhelminthes in the phylogenetic system of the Bilateria. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships in lower invertebrates. The systematics association special vol 28. Clarendon Press, Oxford, pp 168–180
Baccetti B, Afzelius BA (1976) The biology of the sperm cell. Monographs in developmental biology 10. Karger, Basel München Paris London New York Sydney, 254 pp
Dales RP (1962) The polychaete stomodeum and the inter-relationships of the families of Polychaeta. Proc Zool Soc Lond 139:389–428
Eibye-Jacobsen D, Kristensen RM (1994) A new genus and species of Dorvilleidae (Annelida, Polychaeta) from Bermuda, with a phylogenetic analysis of Dorvilleidae, Iphitimidae and Dinophilidae. Zool Scr 23:107–131
Ferraguti M (1984) The comparative ultrastructure of sperm flagella central sheath in Clitellata reveals a new autapomorphy of the group. Zool Scr 13:201–207
Ferraguti M, Lanzavecchia G (1977) Comparative electron microscopic studies of muscle and sperm cells in Branchiobdella pentodonta Whitman and Bythonomus lemani Grube (Annelida Clitellata). Zoomorphologie 88:19–36
Franzén Å (1956) On spermiogenesis, morphology of the spermatozoon, and biology of fertilization among invertebrates. Zool Bidr Uppsala 31:355–482
Franzén Å (1974) Sperm ultrastructure in some Polychaeta. In: Afzelius BA (ed) The functional anatomy of the spermatozoon. Pergamon Press, Oxford New York, pp 267–278
Franzén Å (1977) Ultrastructure of spermatids and spermatozoa in Archiannelida. Zoon 5:97–105
Franzén Å, Rice SA (1988) Spermatogenesis, male gametes and gamete interactions. In: Westheide W, Hermans CO (eds) The ultrastructure of Polychaeta. Microfauna marina 4. Gustav Fischer, Stuttgart New York, pp 309–333
Franzén Å, Sensenbaugh T (1984) Fine structure of spermiogenesis in the archiannelid Nerilla antennata. Vidensk Medd Dan Naturhist Foren 145:23–36
Garavaglia C, Donin CLL, Lanzavecchia G (1974) Ultrastructural morphology of spermatozoa of Hirudinea. J Submicrosc Cytol Pathol 16:229–244
Gerlach SA (1952) Zur Kenntnis der Archianneliden des Mittelmeeres. Kiel Meeresforsch 9:248–251
Graebner I (1969) Vergleichende elektronenmikroskopische Untersuchung der Spermienmorphologie und Spermiogenese einiger Gnathostomula-Arten: Gnathostomula paradoxa (Ax 1956), Gnathostomula axi (Kirsteuer 1964), Gnathostomula jenneri (Riedl 1969). Mikroskopie 24:131–160
Hatschek B (1893) System der Anneliden, ein vorläufiger Bericht. Lotos (Prague) 13:123–126
Heider K (1922) Über Archianneliden. Sitzungsber Akad Wiss Phys Math Kl Berlin: 39–44
Hermans CO (1969) The systematic position of the Archiannelida. Syst Zool 18:85–102
Jamieson BGM (1983a) Spermiogenesis in the oligochaetoid polychaete, Questa (Annelida, Questidae). Zool Scr 12:179–186
Jamieson BGM (1983b) The ultrastructure of the spermatozoon of the oligochaetoid polychaete Questa sp. (Questidae, Annelida) and its phylogenetic significance. J Ultrastruct Res 84:238–251
Jamieson BGM (1984) A phenetic and cladistic study of spermatozoal ultrastructure in the Oligochaeta (Annelida). Hydrobiol 115:3–13
Jamieson BGM (1986) Onychophoran-euclitellate relationships: evidence from spermatozoal ultrastructure. Zool Scr 15:141–155
Jamieson BGM, Rouse GW (1989) The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biol Rev Cambridge Philos Soc 64:93–157
Jamieson BGM, Erséus C, Ferraguti M (1987) Parsimony analysis of the phylogeny of some Oligochaeta (Annelida) using spermatozoal ultrastructure. Cladistics 3:145–155
Jouin C (1978) Spermatozoide non flagellé et fecondation externe chez Protodriloides symbioticus (Giard) (Annélides Polychètes, Archiannélides). Vie Milieu Sér A 28–29:473–487
Kristensen RM, Niilonen T (1982) Structural studies on Diurodrilus Remane (Diurodrilidae fam. n.), with description of Diurodrilus westheidei sp. n. from the Arctic interstitial meiobenthos, W. Greenland. Zool Scr 11:1–12
Kristensen RM, Nørrevang A (1977) On the fine structure of Rastrognathia macrostoma gen. et sp. n. placed in Rastrognathiidae fam. n. (Gnathostomulida). Zool Scr 6:27–41
Mock H (1981) Zur Kenntnis von Diurodrilus subterraneus (Polychaeta, Dinophilidae) aus dem Sandhang der Nordseeinsel Sylt. Helgol Meeresunters 34:329–335
Nielsen C (1995) Animal evolution: interrelationships of the living phyla. Oxford Univ Press, Oxford
Nordheim H von (1987) Anatomie, Ultrastruktur und Systematik der Gattung Protodrilus (Annelida, Polychaeta). PhD Thesis, Osnabrück University, 300 pp
Nordheim H von (1989) Vergleichende Ultrastrukturuntersuchungen der Eu- und Paraspermien von 13 Protodrilus-Arten (Polychaeta, Annelida) und ihre taxonomische und phylogenetische Bedcutung. Helgol Meeresunters 43:113–156
Nørrevang A (1970) The position of Pogonophora in the phylogenetic system. Z Zool Syst Evolutionsforsch 8:161–172
Orrhage L (1974) Über die Anatomie, Histologie und Verwandtschaft der Apistobranchidae (Polychaeta Sedentaria) nebst Bemerkungen über die systematische Stellung der Archianneliden. Z Morphol Tiere 79:1–45
Pfannenstiel H-D, Grünig C (1990) Spermatogenesis and sperm ultrastructure in the polychaete genus Ophryotrocha (Dorvilleidae). Helgol Meeresunters 44:159–171
Purschke G (1993) Structure of the prostomial appendages and the central nervous system in the Protodrilida (Polychaeta). Zoomorphology 113:1–20
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
Remane A (1925) Diagnosen neuer Archianneliden. Zool Anz 65: 15–17
Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 23:111A
Riedl R (1969) Gnathostomulida from America. First record of the new phylum from North America. Science 163:445–452
Rieger RM (1980) A new group of interstitital worms, Lobatocerebridae nov. fam. (Annelida) and its significance for metazoan phylogeny. Zoomorphologie 95:41–84
Rieger RM (1991a) Jennaria pulchra, nov. gen. nov. spec., eine den psammobionten Anneliden nahestehende Gattung aus dem Küstengrundwasser von North Carolina. Ber nat-med Verein Innsbruck 78:203–215
Rieger RM (1991b) Neue Organisationstypen aus der Sandlückenraumfauna: die Lobatocerebriden und Jennaria pulchra. Verh Dtsch Zool Ges 84:247–259
Rieger RM, Tyler S (1979) The homology theorem in ultrastructural research. Am Zool 19:655–666
Rieger RM, Tyler S (1985) Das Homologietheorem in der Ultrastrukturforschung. In: Ott JA, Wagner GP, Wuketits FM (eds) Evolution, Ordnung und Erkenntnis. Parey, Hamburg Berlin, pp 21–36
Rouse GW (1988a) An ultrastructural study of the spermatozoa of Eulalia sp. (Phyllodocidae), Lepidonotus sp. (Polynoidae), Lumbrineris sp. (Lumbrineridae) and Owenia fusiformis (Oweniidae). Helgol Meeresunters 42:67–78
Rouse GW (1988b) An ultrastructural study of the spermatozoa from Prionospio cf. queenslandica and Tripolydora sp.: Two spionid polychaetes with different reproductive methods. Acta Zool (Stockholm) 69:205–216
Rouse GW, Jamieson BGM (1987) An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complanata (Amphinomidae), Clymenella sp., and Micromaldane sp. (Maldanidae), with definition of sperm types in relation to reproductive biology. J Submicrosc Cytol Pathol 19:573–584
Scharnofske P (1986) Ultrastructure of sperm morphology of Trilobodrilus axi und T. heideri (Dinophilidae, Polychaeta). Helgol Meeresunters 40:419–430
Sterrer W, Mainitz M, Rieger RM (1985) Gnathostomulida: Enigmatic as ever. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origins and relationships in lower invertebrates. The systematics association special vol 28. Clarendon Press, Oxford, pp 181–199
Westheide W (1984) Genesis and structure of the modified spermatozoon in the interstitial polychaete Hesionides arenaria. Biol Cell 50:53–65
Westheide W (1985) The systematic position of the Dinophilidae and the archiannelid problem. In: Morris SC, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. The systematics association special vol 28. Clarendon Press, Oxford, pp 310–326
Westheide W (1987) Progenesis as a principle of meiofauna evolution. J Nat Hist 21:843–854
Wingstrand KG (1972) Comparative spermatology of a pentastomid, Raillientiella hemidactyli, and a branchiuran crustacean, Argulus foliaceus, with a discussion of pentastomid relationships. K Dan Vidensk Selsk Biol Skr 19(4):1–72
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Kristensen, R.M., Eibye-Jacobsen, D. Ultrastructure of spermiogenesis and spermatozoa in Diurodrilus subterraneus (Polychaeta, Diurodrilidae). Zoomorphology 115, 117–132 (1995). https://doi.org/10.1007/BF00403260
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DOI: https://doi.org/10.1007/BF00403260