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Spermiogenesis in Mimagoniates Barberi (Teleostei: Ostariophysi: Characidae), an Oviparous, Internally Fertilizing Fish Anna Pecio and Jan Rafinâski

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Spermiogenesis in Mimagoniates Barberi (Teleostei: Ostariophysi: Characidae), an Oviparous, Internally Fertilizing Fish Anna Pecio and Jan Rafinâski Acta Zoologica (Stockholm) 80: 35±45 (January 1999) Spermiogenesis in Mimagoniates barberi (Teleostei: Ostariophysi: Characidae), an oviparous, internally fertilizing fish Anna Pecio and Jan RafinÂski Abstract Institute of Zoology Pecio, A. and Rafin ski, J. 1999. Spermiogenesis in Mimagoniates barberi Department of Comparative Anatomy (Teleostei: Ostariophysi: Characidae), an oviparous, internally fertilizing fish. Jagiellonian University Ð Acta Zoologica (Stockholm) 80: 35±45 Ingardena 6 PL 30060 KrakoÂw The ultrastructure of spermiogenesis of Mimagoniates barberi (Characidae), Poland an internally fertilizing oviparous species is described. Spermiogenesis involves conspicuous changes of the topography of the cellular constituents Keywords: and modifications of their shape. The round nucleus elongates to become a spermiogenesis, ultrastructure, fish, very long flat plate. The long axis of the nucleus establishes the polarity of Mimagoniates, Glandulocaudinae, internal fertilization the spermatid and spermatozoon. The nucleus does not rotate and, as a consequence, the centrioles are located at the proximal tip of the spermato- Accepted for publication: zoon and the flagellum runs parallel to the long axis of the nucleus. Mito- 21 July 1998 chondria and most of the cytoplasm are shifted to the pole opposite the centrioles. The proximal portion of the flagellum is located in a long cytoplasmic canal which shortens during spermiogenesis and is free for most of its length in the mature spermatozoon flagellum. In the cytoplasm of elongated spermatids, close to the nuclear membrane, numerous micro- tubules appear which run from the centriolar pole to the mitochondrial pole forming a microtubular manchette. The microtubules persist in mature spermatozoa. It is concluded that the highly specialized structure of the spermatozoon of M. barberi is the result of only few developmental modifi- cations of spermiogenesis. Anna Pecio, Jan Rafin ski, Institute of Zoology, Department of Comparative Anatomy, Jagiellonian University, Ingardena 6, PL 30060 Krakow, Poland. E-mail: [email protected] The evolution of special structural features of Introduction spermatozoa of internally fertilized fishes must have Structure of fish spermatozoa is extremely diverse involved modifications of the process of spermiogenen- (Jamieson 1991). This diversity can be explained at least sis. Compared with the wealth of information on sper- partly by the diversity of modes of reproduction in fishes. matozoon structure, there are relatively few studies on Most externally fertilized teleosts have a simple type of the fish spermiogenesis. Most of these studies described spermatozoon, called aquasperm, characterized by a either spermiogenesis in fishes with simple spermatozoa roundish head and a short neck region with few mitochon- or in viviparous fishes belonging to advanced fishes of dria (Jamieson 1991; Mattei 1991). In contrast, the group Acanthopterygii (Billard 1970; Mattei 1970; spermatozoa of many internally fertilized teleosts have an Mattei and Mattei 1974; Grier 1975; Brusle 1981; elongated head and other derived features. These was Billard 1983; Billard 1986; Gwo and Gwo 1993). Here shown for example for groups which contain both we present results of an ultrastructural study of spermio- oviparous and viviparous species like Poeciliidae and Ze- genesis in Mimagoniates barberi Regan 1907, a small narchopteridae (Jamieson and Grier 1993). freshwater characid fish from streams of Paraguay. This q 1999 The Royal Swedish Academy of Sciences 35 Spermiogenesis in the teleost Mimagoniates barberi . Pecio and RafinÂski Acta Zoologica (Stockholm) 80: 35±45 (January 1999) species is oviparous but females are inseminated matocytes are spheroid and their shape changes subse- internally (Pecio and Rafin ski 1994). This is a rare mode quently into ovoid, which in later stages of of reproduction in teleosts (Breder and Rosen 1966), spermiogenesis become even more elongated though internal fertilization must have preceded the (Fig. 1A,B). Mitochondria in secondary spermatocytes evolution of viviparity. Mimagoniates barberi belongs to are numerous and the Golgi apparatus is close to the Glandulocaudinae, a small group of oviparous South centriole (Fig. 2A). Clumped or slightly mottled American characids which all practice internal insemina- chromatin of the spermatocyte changes into more evenly tion (Weitzman and Fink 1985; Burns et al., 1995). The granular chromatin typical of early spermatids. The spermatozoon of Mimagoniates barberi has many derived spermatids are interconnected by cytoplasmic bridges, features when compared with spermatozoa of other spaces between them are partly filled with an electron characids with external fertilization (Pecio and Rafin ski dense material (Fig. 2B,C). The diameter of a chromatin 1994). The sperm head is highly elongated, its long axis granuleisatthisstage 40 nm. The nucleus remains is not a continuation of the flagellar axis but runs more more or less spherical but the cell is already polarized. A or less paralell to the flagellum. Live spermatozoa are few, large mitochondria are shifted to one side of the flail-shaped and move with the centriolar part ahead. cell, the proximal centriole is in close contact with the There is no midpiece and the mitochondria are located nuclear membrane. The flagellum is situated within a on the posterior tip of the head. Such spermatozoon relatively short cytoplasmic canal (Fig. 2D). As the structure seems to be unique within Ostariophysi ± the nucleus of the spermatids elongates the cytoplasmic largest group of extant freshwater teleosts (Jamieson canal also elongates (Figs 2E, 3A). The flagellum is at 1991). Elongated spermatozoa have also been found in an angle of 458 relative the long axis of the nucleus, other glandulocaudine genera (Burns et al., 1995). The which shows a more or less flattened surface on the side present study gives the first description of the spermio- of the flagellum. Large flat cisternae develop parallel to genesis in this most unusual group of fishes. the flattened nucleus surface. The cisternae are often associated with the Golgi apparatus and other large vesicles (Fig. 3 B-D). At this stage the spermatid shows Materials and Methods a clear bilateral symmetry and polarity. Its long axis is defined not only by the shape of the nucleus but also by Sexually active males of M. barberi were taken from a the position of the proximal centriole which is situated breeding colony kept at our Department. Testes were on the apical side of the spermatid and by the position excised after the fishes were killed by an overdose of of the mitochondria on the opposite side. Most of the tricaine methanesulphonate (MS-222). Small pieces of cytoplasm is concentrated on the mitochondrial, either spermatogenic or aspermatogenic tissue of the testis posterior pole of the spermatid and on the flagellar side were fixed in 3% glutaraldehyde in cacodylate buffer (Fig. 3A). (pH = 7.4), post-fixed in 1% osmium tetroxide, The elongation of the nucleus and the spermatid dehydrated through ethanol series and embedded in Epon proceeds further. At this stage the nucleus is more or less 812. The ultrathin sections, stained with uranyl acetate tear-shaped (Fig. 4A). The nucleus has an elongated tip at and lead citrate, were examined in a JEOL JEM-100Sx the centriolar pole, while its mitochondrial tip is wide and electron microscope. obtuse. The chromatin is granular but the granules have For scanning electron microscopy, testes of four enlarged to 60±70 nm in diameter. The cytoplasm is specimens were fixed as for TEM, dehydrated in acetone, almost completely shifted to the mitochondrial pole and to critical-point dried, fractured, sputter-coated with gold the flagellar side of the spermatid (Fig. 4A). The flagellar and viewed in a JEOL JSM 35. canal elongates and reaches the mitochondrial pole (Fig. 4F). Results At later stages numerous microtubules appear in the cytoplasm. They originate in two groups situated laterally The testis of a mature M. barberi is composed of two to the distal centriole and continue along the centriolar- parts. In the anterior part of the testis spermatogenesis mitochondrial axis of the spermatid (Fig. 4 B-G). Closer takes place, whereas its caudal portion is devoid of any to the centriolar pole many rows of microtubules surround spermatogenic tissue and functions as a sperm storage the nucleus. They are also found in the cytoplasm adjacent organ(PecioandRafin ski, 1994). Germ cells are to the flagellar canal (Fig. 4 C,D). Further in the direction confined to cysts located within the seminiferous of the mitochondrial pole, microtubules form a single row tubules. Earlier stages of spermatogenesis in M. barberi approaching the nuclear membrane and reach the do not show any peculiarities; spermatogonia and sper- cytoplasm of the mitochondrial tip of the spermatid (Fig. 4 matocytes are very similar to those described in other E,F). The spermatids are still connected by the teleosts (Billard 1983; Selman and Wallace 1986). Sper- cytoplasmic bridges (Fig. 4G). 36 q 1999 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 80: 35±45 (January 1999) Pecio and RafinÂski . Spermiogenesis in the teleost Mimagoniates barberi Fig. 1.ÐThe inner surface of the spermatogenic cysts in SEM. Ð A, The primary spermatocytes (sc) situated in depressions of Sertoli cells (Sc). Ð B, Spherical (ss), ovoid (so) and strongly elongated (se) spermatids in separate cysts during
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