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PROOFS Mais Ampla Na Ordem Neotropical Ichthyology, 3(3):401-410, 2005 Copyright © 2005 Sociedade Brasileira de Ictiologia Comparative description and discussion of spermiogenesis and spermatozoal ultrastructure in some species of Heptapteridae and Pseudopimelodidae (Teleostei: Siluriformes) Irani Quagio-Grassiotto, Maria Angélica Spadella, Márcio de Carvalho, and Claudio Oliveira The data obtained in the present study on spermiogenesis and spermatozoal ultrastructure of Pseudopimelodidae and Heptapteridae show that they share some characteristics, but greatly differ from each other. The main differences are the occurrence of type I spermiogenesis in Pseudopimelodidae and type III in Heptapteridae, the presence of nuclear fossa in Pseudopimelodidae and its absence in Heptapteridae, the presence of long midpiece in Pseudopimelodidae and short midpiece in Heptapteridae, the presence of cytoplasmic canal in Pseudopimelodidae and its absence in Heptapteridae, the presence of many large vesicles in the midpiece of Pseudopimelodidae and the presence of very long vesicles placed in the peripheral distal region in Heptapteridae, and mitochondria distributed all over the midpiece in Pseudopimelodidae, and very close to the nucleus in Heptapteridae. Heptapteridae and Pimelodidae share several characteristics, such as type III spermiogenesis, a similar chromatin condensation pattern, and the absence of nuclear fossa and flagellar lateral fins. The spermatozoa of Pseudopimelodidae is more similar to those of Siluridae. However, the absence of additional data on spermiogenesis and spermatozoa in siluriforms still limits a broader discussion in the order. Os dados obtidos no presente estudo sobre a ultraestrutura da espermiogênese e dos espermatozóides de Pseudopimelodidae e Heptapteridae mostram que eles compartilham algumas características, mas são bastante diferentes uns dos outros. As principais diferenças são a ocorrência de espermiogênese do tipo I em Pseudopimelodidae e do tipo III em Heptapteridae, a presença de fossa nuclear em Pseudopimelodidae e sua ausência em Heptapteridae, a presença de uma peça intermediária longa em Pseudopimelodidae e uma peça intermediária curta em Heptapteridae, a presença de um canal citoplasmático em Pseudopimelodidae e sua ausência em Heptapteridae, a presença de muitas vesículas grandes na peça intermediária de Pseudopimelodidae, e a presença de vesículas muito alongadas e dispostas em posição periférica distal em Heptapteridae e mitocôndrias distribuídas em toda a peça intermediária de Pseudopimelodidae e muito próximas ao núcleo em Heptapteridae. Heptapteridae e Pimelodidae compartilham várias características como a espermiogênese do tipo III, o mesmo padrão de condensação da cromatina e a ausência de fossa nuclear e projeções laterais ou fins. O espermatozóide de Pseudopimelodidae é mais similar aos dos Siluridae, porém a ausência de dados adicionais sobre a espermiogênese e o espermatozóide de outros siluriformes ainda limitam uma discussãoPROOFS mais ampla na ordem. Key words: catfish, spermatid, sperm, structure, phylogeny. Introduction is a general consensus that the family Diplomystidae is the sister group of all other Siluriforms. According to the phylog- Siluriformes comprise the most diverse and widely distrib- eny proposed by Britto (2003), the families Pimelodidae, uted ostariophysan group and represent about 32% of all Heptapteridae and Pseudopimelodidae belong to a monophyl- freshwater fishes (Teugels, 1996). The relationships among etic clade that includes Anchariidae, Austroglanididae, catfish families have long been studied, but the higher-level Bagridae, Claroteinae, Cranoglanididae, Doradoidei, phylogeny of siluriforms is still controversial (Diogo, 2003). It Pangasiidae, Schilbidae, and Horabagrus. In his phylogeny, Depto. de Morfologia, Instituto de Biociências - Botucatu, Universidade Estadual Paulista - UNESP, C.P. 510 , 18618-000 Botucatu, SP, Brazil. e-mail: [email protected] 401 402 Spermiogenesis and spermatozoal ultrastructure in some species of Heptapteridae and Pseudopimelodidae Pseudopimelodidae and Heptapteridae appear as a monophyl- Materials and Methods etic group, as well as the most basal group of this clade. Pimelodidae occupy a more derived position and is the sister- The present study was conducted with five to ten adult group of the clade formed by Anchariidae, Austroglanididae, males of Rhamdia quelen (Heptapteridae) (catalog number: Bagridae, Claroteinae, Cranoglanididae, Pangasiidae, LBP 1345) and Microglanis aff. parahybae (Pseudopi- Schilbidae and Horabagrus (Britto, 2003). melodidae) (catalog numbers: LBP 1193, LBP 1308 and LBP Pseudopimelodidae may be considered the least known 1315) collected from the rio Araquá, Botucatu, São Paulo, and one of the smallest families of neotropical freshwater Brazil (22°47.135’S, 48°28.892’ W) and Pimelodella gracilis catfishes (Shibatta, 2003). Lundberg et al. (1991) first demon- (Heptapteridae) (catalog number: LBP 1741) collected from strated the monophyly of this group and suggested the exist- the rio Alambari, Botucatu, São Paulo, Brazil (22°56’08'’ S, ence of a relationship between Pseudopimelodidae and the 48°19’15'’ W). The fishes were identified and kept in the fish basal Heptapteridae. This hypothesis was corroborated by collection of Laboratório de Biologia e Genética de Peixes Britto (2003). The family Heptapteridae comprises small to (LBP), Departamento de Morfologia, Instituto de Biociências, medium-sized fishes and forms one of the largest group of UNESP, Botucatu, São Paulo, Brazil. Neotropical catfishes (Bockmann & Guazzelli, 2003). Gonad fragments from newly sacrificed fish were fixed Bockmann (1998) considered Goeldiella as the sister group overnight in 2% glutaraldehyde and 4% paraformaldehyde in of all other Heptapteridae. The remaining Heptapteridae were 0.1 M Sorensen phosphate buffer, pH 7.4. The material was divided into three clades: one composed by Rhamdia quelen, post-fixed in the dark for 2 hours in 1% osmium tetroxide in another by R. laticauda and Pimelodella, and the other by the same buffer, stained in block with an aqueous solution of the remaining species (Bockmann, 1998). 5% uranyl acetate for two hours, dehydrated in acetone, em- Although the current knowledge of the relationship pat- bedded in araldite, and sectioned and stained with a satu- tern among Siluriformes has been acquired on the basis of rated solution of uranyl acetate in 50% alcohol and lead cit- morphological characters, other data seem to be potentially rate. Electron micrographs were obtained using a Phillips - useful for the study of this group. Within this framework, CM 100 transmission electron microscope. spermatogenesis and spermatozoal ultrastructure have been studied in several fish groups (Jamieson, 1991; Mattei, 1970; Results 1991) and the usefulness of this type of data in the clarifica- tion of the relationship among some families has been fully General observations. In the species analyzed, spermiogen- recognized. Based on the phylogeny proposed by Britto esis occurs in cysts in the germinative epithelium. These cysts (2003), with the exception of Sisoroidea, Amphiliidae, and consist of a group of germ cells at the same developmental Loricarioidea, detailed descriptions of spermatozoa are cur- stage, which are surrounded by cytoplasmic processes of rently available only for some species of the following catfish Sertoli cells. In the cysts, the early spermatids are intercon- families: Diplomystidae (Quagio-Grassiotto et al., 2001), nected by cytoplasmic bridges resultant from incomplete cy- Clariidae (Mansour et al., 2002), Siluridae (Emel’yanova & tokinesis of both the anterior mitotic and the meiotic divi- Makeyeva, 1991b; Kwon et al., 1998; Lee & Kim, 2001), sions. In all the species, spermatozoa exhibit a head, a Ictaluridae (Jaspers et al., 1976; Poirier & Nicholson, 1982; midpiece, and one tail or flagellum. The head does not have Emel’yanova & Makeyeva, 1991a,b), Auchenipteridae (Burns an acrosomal vesicle. et al., 2002), Pimelodidae (Quagio-GrassiottoPROOFS & Carvalho, 2000; Quagio-Grassiotto & Oliveira, in press) and Bagridae Pseudopimelodidae spermiogenesis. In M. aff. parahybae early (Emel’yanova & Makeyeva, 1991b; Lee, 1998; Kim & Lee, spermatids, the cytoplasm symmetrically encircles the nucleus, 2000). General information is found about the spermatozoa of which shows diffuse homogenous chromatin, and has a circu- Heteropneustidae (Nath & Chand, 1998), Malapteruridae, lar outline. The centriolar complex lies laterally to the nucleus Mochokidae, Schilbidae, and Ariidae (Mattei, 1991-schematic and anchors to the plasma membrane. The proximal centriole is drawings), and Conorhynchus conirostris (Lopes et al., 2004). anterior, oriented end-by-end and slightly oblique in relation There is no information about the sperm cell of the to the distal centriole. The distal centriole differentiates into Anchariidae, Auchenoglanidinae, Austroglanididae, the basal body and forms the flagellum. The centriolar complex Chacidae, Claroteinae, Cranoglanididae, Doradidae, moves toward the nucleus, carrying along the plasma mem- Heptapteridae, Horabagrus, Pangasiidae, Plotosidae, or brane and the initial segment of the flagellum, which invagi- Pseudopimelodidae. nates. The cytoplasmic channel, a space between the flagellum Considering their informative phylogenetic potential, the and the plasma membrane, is then formed (Figs. 1A-H). A de- ultrastructural characters of both spermiogenesis and sper- pression is formed in the nuclear
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