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Spermiogenesis in Seison Nebaliae (Rotifera, Seisonidea): Further Evidence of a Rotifer-Acanthocephalan Relationship*

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Spermiogenesis in Seison Nebaliae (Rotifera, Seisonidea): Further Evidence of a Rotifer-Acanthocephalan Relationship* Tissue & Cell, 1999 31 (4) 428–440 © 1999 Harcourt Publishers Ltd Article no. tice.1999.0012 Tissue&Cell Spermiogenesis in Seison nebaliae (Rotifera, Seisonidea): further evidence of a rotifer-acanthocephalan relationship* M. Ferraguti, G. Melone Abstract. The spermatozoa of Seison nebaliae are filiform cells about 70 µm long with a diameter of 0.6 µm. They have a slightly enlarged head, 2.5 µm long, followed by a long cell body. The flagellum starts from the head, and runs parallel to the cell body, contained in a groove along it. The head contains an acrosome, two large, paired para-acrosomal bodies, the basal body of the flagellum and the anterior thin extremity of the nucleus. The cell body contains the main portion of the nucleus, a single mitochondrion located in its distal portion, and many accessory bodies with different shapes. The flagellum has a 9 + 2 axoneme. The study of spermiogenesis shows the Golgian origin of the acrosome and the para-acrosomal bodies and reveals some peculiarities: a folding of the perinuclear cisterna is present between the proacrosome and the basal body of the flagellum in early spermatids and the flagellum runs in a canal inside the spermatid cytoplasm. The basal body migrates anteriorly. These char- acters are shared partly by the Rotifera Monogononta and, to a large extent, by the Acanthocephala studied so far. Many details of the spermiogenetic process are identical to those of Acanthocephala, thus suggesting that the processes in the two taxa are homologous. © 1999 Harcourt Publishers Ltd. Keywords: Seison, rotifera, spermatozoa, spermiogenesis, phylogeny Introduction of rotifers in the debate on the phylogeny of lower Metazoa, the morphology of their spermatozoa, at ultrastructural The three classes of the phylum Rotifera, i.e. Seisonidea, level, is known only for five species (Melone & Ferraguti, Monogononta, and Bdelloidea, are characterized, inter alia, 1998). Even poorer is our knowledge of the ultrastructure by their modalities of reproduction: Bdelloidea are obligate and sperm morphology in Seisonidea, a class composed by parthenogens, Monogonota reproduce mainly by partheno- two species only, belonging to the same genus, Seison. Both genesis, with rare periods of arrhenothoky with the produc- species, Seison nebaliae (Grube, 1861) and S. annulatus tion of dwarf haploid males, whereas only in Seisonidea (Claus, 1876) live epizoic on Nebalia bipes (O. Fabricius, there is a bisexual reproduction with regular, contemporary 1780) (Crustacea, Leptostraca). After the old papers by presence of males and females. Spermatozoa are thus Plate (1888), de Beauchamp (1909), Illgen (1916) and present, among rotifers, only in species of Monogononta Remane (1929–1933), mainly concerned with the anatomy and Seisonidea. of the animals, the fine structure of male germ cells was Despite the high number of monogonont species studied with the scanning electron microscope only by Ricci (>1500), their ecological importance, and the key position et al. (1993) and with the transmission electron microscope Dipartimento di Biologia, Università di Milano, 26, via Celoria, I-20133, *Since the submission of this paper, a paper has been published (Ahlrichs, Milano, Italy WH 1998. Spermatogenesis and ultrastructure of the spermatozoa of S. nebaliae [Syndermata]. Zoomorphology, 118, 255–261). The results Received 3 December 1998 Accepted 19 January 1999 presented by Ahlrichs are consistent with the authors’, with some minor discrepancies. The conclusions reached by the author about sister-group Correspondence to: M. Ferraguti. Fax: +39 2 2660 4462; relationships of Seison and Acanthocephala are also similar to those of the E-mail: [email protected] present paper, and to those of Melone and Ferraguti (1998). 428 SPERMIOGENESIS IN SEISON NEBALIAE 429 by Ahlrichs (1995a) in his Ph D thesis. A general ultrastruc- days, then washed in 0.1 M cacodylate buffer, postfixed in tural description is provided in the review by Melone and cacodylate buffered 1% osmium tetroxide, briefly washed Ferraguti (1998). A poor knowledge of Seison spermatozoa in distilled water, pre-stained for 2 h en bloc in 2% aqueous is particularly regrettable for two reasons: first, Seisonidea uranyl acetate, dehydrated in a graded ethanol series, and may be the most ancient rotifer taxon (Wallace & Colburn, embedded in Spurr resin. Thin sections, obtained with an 1989; Wallace & Snell, 1991) and second the biology of LKB Ultrotome III and V, were stained in lead citrate, male gametes in Seison appears particularly complex, with carbon coated, and observed with a Jeol 100 XS electron spermatozoa encysted one by one at maturity, then trans- microscope. ferred encysted to the female where they ‘unroll’ and travel into the oviduct to the germarium (Ricci et al., 1993). Scanning electron microscopy (SEM) Spermatozoa are considered as an important source of Whole narcotized animals were fixed with SPAFG, as characters for phylogenetic reconstructions (Jamieson et al., reported in the previous paragraph, then washed in distilled 1995) but, on the other hand, our knowledge of pseudo- water. After the dehydration in a graded ethanol series, the coelomate sperm is full of gaps. The aim of this paper is to specimens were critical-point dried with CO2, coated with describe the ultrastructure of the spermatozoa of S. nebaliae gold, and observed under a Cambridge Stereoscan 250 Mk2. both at complete maturity and in the encysted form, to The sperm material was isolated on coverslips and outline some important steps of spermiogenesis, and to stained with DAPI. After the observation under the optical compare the morphological features of seisonidean sperm to microscope, the coverslips where processed with hexam- those of the other rotifers and the other lower metazoan ethyldisilazane (Melone & Ferraguti, 1994), glued with phyla. silver paint to SEM stubs, coated with gold and observed under a Cambridge Stereoscan 250 Mk2. Materials and methods Results Nebalia bipes were collected by traps of enrolled fish nets, containing dead fishes, and left for 2–3 days on the sea The male genital apparatus of S. nebaliae is a prominent U- bottom in Venice lagoon and in Puerto de Andratx shaped structure almost filling the trunk of the animal. It is (Majorca, Spain). Different percentages of collected formed by two large paired sac-like testes situated laterally Nebalia bipes were associated with Seison nebaliae: to the gut, and connected posteriorly to a common vas 60–80% in Venice lagoon and 10–20% in Puerto de deferens. This last folds forward, crosses a pear-like organ Andratx. The rotifers, narcotized with marcaine and gently dorsal to the stomach, and finally outlets in the cloacal aper- removed from the host, were examined under a stereomicro- ture, situated at the connection between the neck and trunk scope. The adult male seisonids, easily recognisable by the of the animals (Remane, 1929–1933). Mature spermatozoa size (about 1 mm length) and by the humped trunk (Fig. can be found in the testes and in the first tract of the vas 1C), were dissected in sea water with thin tungsten needles deferens, whereas the spermiogenesis can be examined in to isolate mature spermatozoa for in vivo observation of the the testes. In the pear-like organ the mature spermatozoa are movement and for observations under optical and scanning encysted one by one in a process lasting 90 s (Illgen, 1914). electron microscopes, after fixation. There and in the following tract of the vas deferens we have examined the encysted spermatozoa. Optical microscopy Living spermatozoa, isolated in sea water, were observed Mature spermatozoa (Figs 1–4) under a Leitz Dialux phase contrast microscope and the The spermatozoon of S. nebaliae is a thin, filiform cell 70 sperm movement was recorded on a U-matic videocassette. µm long with a fairly constant diameter of approximately Cysts, mature spermatozoa and encysted spermatozoa were 0.6 µm (Fig. 1A). The diameter is only slightly increased to isolated on coverslips coated with poly-1-lysine, fixed with 0.8 µm at one of the extremities, about 2.5 µm long, a sucrose-picric acid-paraformaldehyde-glutaraldehyde showing a characteristic hood shape (Figs 1B, D & 2B). solution (SPAFG: Ermak & Eakin 1976) 1200 mOsm When observed in sea water the spermatozoa wave actively (Melone & Ferraguti, 1994), stained with 4,6-Diamidino-2 with the hood anteriorly. The movement is particularly phenylindole (DAPI) solution (2 µg/ml) for nuclear identifi- accentuated in the sperm region opposite to the hood. cation and observed under a Leitz DM RB Nomarski inter- Following Justine’s convention about Platyhelminthes ference contrast and fluorescence microscope. (1995), we consider the hood-shaped slightly enlarged portion as the head, and will distinguish it, in the following Transmission electron microscopy (TEM) description, from the cell body. The males of S. nebaliae were fixed at room temperature The head is a bilaterally symmetric structure containing with 0.1 M cacodylate buffered SPAFG. The worms were apically a conical vesicle (hereafter: acrosome) under which left in the fixative for different times, from 2 h to several the flagellum is inserted with its basal body (Figs 2A, B & 430 FERRAGUTI, MELONE Fig. 1 A A single spermatozoon as seen under SEM. The posterior extremity is recognizable for its coiled arrangement. B A head at higher magnifica- tion (compare to Fig. 2 A, B). C Seison nebaliae (m, male; f, female) on its host, Nebalia bipes. D A group of mature spermatozoa. E Encysted sperma- tozoa. F, G The same mature spermatozoon as seen under Nomarski interference contrast microscope (F) and under the fluorescence microscope after DAPI staining (G). Note that the dye localizes the nucleus all along the cell, with an intenser positivity in the posterior portion. H, I the same microscopic field containing encysted spermatozoa, as seen under the Nomarski interference contrast microscope (H) and under the fluorescence microscope (I) after DAPI staining. The whole spermatozoon is highly coiled, thus the encysted sperm is entirely DAPI-positive.
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