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Araneae, Linyphiidae) 2005. The Journal of Arachnology 33:569±572 ON THE OCCURRENCE OF THE 9 1 0 AXONEMAL PATTERN IN THE SPERMATOZOA OF SHEETWEB SPIDERS (ARANEAE, LINYPHIIDAE) Peter Michalik and Gerd Alberti: Zoologisches Institut und Museum, Ernst-Moritz- Arndt-UniversitaÈt, J.-S.-Bach-Straûe 11/12, D-17489 Greifswald, Germany. E-mail: [email protected] ABSTRACT. In general, ¯agella and cilia of eukaryotes show an axoneme composed of a 9 1 2 microtubular pattern. However, the axoneme of spider spermatozoa is characterized by an exceptional 9 1 3 microtubular pattern, which is known as a synapomorphy of the Megoperculata (Amblypygi, Uropygi and Araneae). In contrast to all other observed spiders, the axoneme of the linyphiid spider Linyphia triangularis, was shown to lack the central microtubules thus representing a 9 1 0 axoneme. In the present study, we investigated the spermatozoa from several linyphiid species of different genera in order to show whether this peculiar pattern also occurs in other linyphiid spiders. Interestingly, in all observed species (Neriene clathrata, N. peltata, Linyphia hortensis, Lepthyphantes sp., Oedothorax gibbosus, Gongylidium ru®pes and Drapetisca socialis) we found the 9 1 0 microtubular pattern in the axoneme. Since this study, although considering still a very limited number of species, includes species from Linyphiinae (Linyphiini and Micronetini) and Erigoninae it seems likely that this pattern is an autapomorphy of Linyphiidae. Keywords: Sperm, phylogeny, axoneme, microtubules The typical and plesiomorphic axoneme aneae (Megoperculata) possess as a synapo- found in eukaryote ¯agella and cilia possess morphy a 9 1 3 pattern (summary in Alberti a91 2 arrangement of the microtubules. 2000; Michalik et al. 2003, 2004, in press and Nevertheless, there is a wide range of modi- further personal observations). Thus it seems ®cations within the axoneme of sperm ¯agel- remarkable, that the linyphiid spider Linyphia la, e.g., in insects (Jamieson et al. 1999). Also triangularis (Clerck, 1757) has an unusual 9 within the Chelicerata a broader range of pat- 1 0 axonemal pattern (Alberti 1990); unfor- terns occurs as shown by the recent species of tunately until now there have been no other the early derivative group, Xiphosura, where ultrastructural observations on Linyphiidae two different patterns are reported (9 1 2 and spermatozoa to know assess if this pattern is 9 1 0; Fahrenbach 1973; Yamamichi & Sek- typical of this taxon. iguchi 1982; Alberti & Janssen 1986). Within In the present study, we investigated the arachnids only the spermatozoa of Scorpiones, spermatozoa of several different linyphiid spi- Uropygi, Amblypygi, Araneae, Pseudoscorpi- ders from the subfamilies Linyphiinae (Liny- ones and Ricinulei possess a ¯agellum (sum- phiini and Micronetini) and Erigoninae to be- mary in Alberti 2000), in contrast to the sper- gin a determination of the generality of this matozoa of Solifugae, Acari, Palpigradi and peculiar axonemal pattern within the Linyphi- Opiliones, which are a¯agellate (the only ex- idae. ception is the opilionid genus Siro which Male specimens of Neriene clathrata (Sun- shows an axoneme during the spermatogene- devall 1830), N. peltata (Wider 1834), Liny- sis; Juberthie et al. 1976; Alberti in press). phia hortensis Sundevall 1830 (Linyphiinae, The typical 9 1 2 pattern occurs only in Scor- Linyphiini); Lepthyphantes sp. (Linyphiinae, piones, Pseudoscorpiones and Ricinulei. How- Micronetini); Oedothorax gibbosus (Black- ever, in Scorpiones aberrant patterns, e.g., 9 wall 1841) and Gongylidium ru®pes (Linnaeus 1 0 and 9 1 1 have also been reported (Hood 1758) (Erigoninae); and Drapetisca socialis et al. 1972; Jespersen & Hartwick 1973; Al- (Sundevall 1833) were dissected and ®xed in berti 1983). The Uropygi, Amblypygi and Ar- 2.5% glutaraldehyde in 0.1 M phosphate buff- 569 570 THE JOURNAL OF ARACHNOLOGY Figures 1±7.ÐSpermatozoa of the observed linyphiid species. 1. Early spermatids of Oedothorax gibbosus with axonemes in crossÐand longitudinal sections. Scale bar 5 1 mm. Inset: Detail of the axoneme of Linyphia hortensis in cross-section showing the 9 1 0 pattern. Scale bar 5 0.1 mm. 2Ð3. Posterior part of an early spermatid in longitudinal section. 2. Neriene clathrata. Scale bar 5 0.25 mm. 3. Lepthyphantes sp. Scale bar 5 0.5 mm. 4Ð6. Late spermatids. 4. Drapetisca socialis. Scale bar 5 1 mm. 5. Gongylidium ru®pes. Scale bar 5 0.5 mm. 6. Neriene peltata. Scale bar 5 0.5 mm. 7. Coiled spermatid of Linyphia hortensis. Scale bar 5 0.5 mm. Abbreviations: Ax 5 axoneme, C 5 centriole, IF 5 implantation fossa, N 5 nucleus, NC 5 nuclear canal (canal containing the acrosomal ®lament). er followed by post®xation in buffered 2% os- scope. Voucher specimens have been depos- mium tetroxide. After rinsing, the specimens ited in the Zoological Museum of the were dehydrated in graded ethanols and em- University of Greifswald. bedded in Araldite or Spurr's resin (Spurr Spermiogenesis starts with spermatids 1969). Ultrathin sections were made on a Lei- which are mainly characterized by a large, ca ultramicrotome and the sections were roundish nucleus lying in a homogenous cy- stained with uranyl acetate and lead citrate toplasm (Fig. 1). The axoneme migrates into (Reynolds 1963). The examination was per- the posterior pole of the nucleus (Figs. 1±4). formed with a Zeiss EM 10A electron micro- The centrioles are orientated in the tandem po- MICHALIK & ALBERTIÐSPERMATOZOA OF LINYPHIIDAE 571 sition (Fig. 2). In all sections, the absence of (1990) that this peculiar pattern might be an the central tubules in the axoneme is obvious autapomorphy of Linyphiidae. Therefore it in all investigated species (Figs. 1±7) and in would be of much interest to know the situ- cross sections, the 9 1 0 axonemal pattern is ation in the supposed sister taxon Pimoidae as evident (Figs. 1 inset, 4±7). Parallel to the mi- well as in the other linyphiid subfamilies (e.g., gration of the axoneme, a deep posterior in- Hormiga 1994a, b; 2000). dentation into the nucleus is formed, the so- ACKNOWLEDGMENTS called implantation fossa (Fig. 1) which is ®lled with dense material at the end of sper- We are very grateful for the assistance of matogenesis (Figs. 4, 7). At the end of sper- Wencke Reiher. Furthermore, we thank Ga- matogenesis the nucleus coils once and the ax- briele Uhl (Bonn) for the provision of the oneme turns around the nucleus in the males of O. gibbosus. For the exact identi®- periphery of the cell (Fig. 7). cation of part of the material we are indebted The occurrence of the 9 1 0 axonemal pat- to Konrad Thaler (Innsbruck).This study was tern is unique among the spermatozoa of Me- ®nancially supported by the German National goperculata and was ®rst shown by Alberti Merit Foundation (grant to PM) and the Ger- (1990) for Linyphia triangularis. In spiders a man Research Foundation (DFG, Al 138/11± 9 1 3 pattern normally occurs and was studied 1). in detail by Dallai et al. (1995). The present LITERATURE CITED 1 study shows the peculiar 9 0 pattern for all Alberti, G. 1983. Fine structure of scorpion sper- observed Linyphiidae. Based on these obser- matozoa (Buthus occitanus; Buthidae, Scorpi- vations many questions arise concerning the ones). Journal of Morphology 177:205±212. function and the phylogenetic impact of this Alberti, G. 1990. Comparative spermatology of Ar- character. Unfortunately, no studies on the aneae. Acta Zoologica Fennica 190:17±34. movement of linyphiid spermatozoa exist. Alberti, G. 2000. Chelicerata. Pp. 311±388. In Pro- However, it was shown from other animal spe- gress in Male Gamete Ultrastructure and Phylog- cies that an axoneme which lacks the central eny. Vol. 8. (B. G. M. Jamieson, ed.). Oxford & tubules can still move. For example, Ishijima IBH Publishing Co. PVT. LTD, Queensland. et al. (1988) compared the beat pattern from Alberti, G. In press. Double spermatogenesis in Chelicerata. Journal of Morphology. Asian and American horseshoe crabs. The Alberti, G. & H.H. Janssen. 1986. On the ®ne struc- Asian species Tachypleus gigas (MuÈller 1785) ture of spermatozoa of Tachypleus gigas (Xip- possess a 9 1 0 axoneme which beats in he- hosura, Merostomata). International Journal of lical waves, in contrast to the planar waves of Invertebrate Reproduction and Development 9: the 9 1 2 axoneme of the American horseshoe 309±319. crab Limulus polyphemus (Linnaeus 1758). Dallai, R., B.A. Afzelius & W. Witalinski. 1995. Similar results were also reported in the de- The axoneme of the spider spermatozoon. Bol- tailed studies of Gibbons et al. (1983, 1985) lettino di Zoologia 62:335±338. on the eel Anguilla anguilla (Linnaeus 1758) Fahrenbach, W.H. 1973. Spermiogenesis in the which possess spermatozoa with a 9 1 0 ax- horseshoe crab Limulus polyphemus. Journal of Morphology 140:31±52. oneme which lacks the central tubules as well Gibbons, B.H., B. Baccetti & I.R. Gibbons. 1985. as other structures, e.g., outer dynein arms, ra- Live and reactivated motility in the 910 ¯agel- dial spokes and spokeheads. The spermatozoa lum of Anguilla sperm. Cell Motility 5:333±350. of the eel beats in helicoidal waves. Hence it Gibbons, B. H., I.R. Gibbons & B. Baccetti. 1983. can be assumed that the spermatozoa of Lin- Structure and motility of the 910 ¯agellum of yphiidae are motile and the movements of the eel spermatozoa. Journal of Submicroscopic Cy- axoneme are different from those of other spi- tology 15:15±20. der spermatozoa that possess a 9 1 3 axo- Hood, R.D., O.F. Watson, T.R. Deason & C.L.B. neme. More investigations are needed to test Benton,Jr. 1972. Ultrastructure of scorpion sper- this hypothesis and clarify the possible in¯u- matozoa with atypical axonemes. Cytobios 5: 167±177. ence (selective advantage?) within the female Hormiga, G.
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