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Comparative Analysis of the Sperm Ultrastructure of Three Species of 2 Sam Noble Oklahoma Museum of Natural Phyllomedusa (Anura, Hylidae)

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Comparative Analysis of the Sperm Ultrastructure of Three Species of 2 Sam Noble Oklahoma Museum of Natural Phyllomedusa (Anura, Hylidae) Acta Zoologica (Stockholm) 85: 257–262 (October 2004) ComparativeBlackwell Publishing, Ltd. analysis of the sperm ultrastructure of three species of Phyllomedusa (Anura, Hylidae) G. C. Costa,1 A. A. Garda,2 R. D. Teixeira,3 G. R. Colli4 and S. N. Báo5 Abstract 1Departamento de Ecologia, Universidade Costa, G.C., Garda, A.A, Teixeira, R.D., Colli, G.R. and Báo, S.N. 2004. de Brasília, 70919–970, Brasília, DF, Brazil; Comparative analysis of the sperm ultrastructure of three species of 2 Sam Noble Oklahoma Museum of Natural Phyllomedusa (Anura, Hylidae). — Acta Zoologica (Stockholm) 85: 257–262 History, Norman, Oklahoma, 73072–7029, USA; 3Departmento de Biologia, We describe the sperm ultrastructure of three species of frogs in the genus Universidade Católica de Brasília, EPCT Phyllomedusa. According to micrographs, total size of the spermatozoon of Q.S. 7, lote 1, Águas Claras, 72030–170, Phyllomedusa hypochondrialis is significantly smaller than those of Phyllomedusa 4 Taguatinga, DF. Brazil; Departamento de bicolor and Phyllomedusa tarsius. The acrosome complex consists of two conical Zoologia, Universidade de Brasília, 70919– structures covering the nucleus, the acrosome vesicle and the subacrosomal 970, Brasília, DF, Brazil; 5Departamento de Biologia Celular, Universidade de Brasília, cone. The subacrosomal cone of P. bicolor and P. tarsius is less electron-dense 70919–970, Brasília, DF, Brazil and appears more granular in transverse section than in P. h ypochondrialis. In P. bicolor and P. tarsius, the nuclear space is reduced and the subacrosomal cone Keywords: fills most of the space between the acrosome vesicle and nucleus. The anterior Hylidae, sperm, ultrastructure, region of the nucleus in the spermatozoa of P. bicolor and P. tarsius ends Phyllomedusa abruptly, while in P. hypochondrialis it is sharp-ended. In P. bicolor and P. tarsius, the axial fibre is much larger than in P. hypochondrialis. The sperm ultrastructure Accepted for publication: of Phyllomedusa appears conservative at the intrageneric level. Future studies on 16 December 2004 the sperm ultrastructure of hylids can provide new insights on the systematics of the group and a larger database for a cladistic analysis. Sônia Nair Báo, Departamento de Biologia Celular, Instituto de Ciências Biológicas, Universidade de Brasília, 70919–970 Brasília, DF, Brazil. E-mail: [email protected] alternative data sets is necessary for a trustworthy phylo- Introduction genetic reconstruction of amphibians (Wake 1993). Several detailed studies on many taxa, including fishes Among amphibians, the first works on sperm ultrastructure (Jamieson 1991; Tanaka et al. 1995), reptiles (Jamieson 1995; described the peculiarities of the cell and made no reference Teixeira et al. 1999), invertebrates (Rouse and Jamieson to any aspect of species ecology or character evolution. Few 1987; Buckland-Nicks 1995) and amphibians (Jamieson recent studies have been conducted on the subject and et al. 1993; Lee and Jamieson 1993; Meyer et al. 1997; associates sperm morphology with fertilization biology Garda et al. 2002) revealed that sperm ultrastructure pro- and phylogeny (Meyer et al. 1997; Scheltinga et al. 2002a). vides an alternative source of useful characters for phyloge- Recently, detailed publications on amphibian sperm netic analysis. Teixeira et al. (1999) analysed the skewness ultrastructure of several families have provided careful of tree length distributions from lizard sperm ultrastructure descriptions such as Leiopelmatidae (Scheltinga et al. 2001), characters and concluded that the data set contained signi- Microhylidae (Scheltinga et al. 2002b) and Leptodactylidae ficant phylogenetic signal. (Amaral et al. 2000). However, there is still a lack of Phylogenetic relationships among anurans are still unclear information on several families and much to be investigated, even among higher taxa. This outcome derives from the especially in the Neotropical realm. Furthermore, little is limited number of characters traditionally employed in phy- know about the variation of sperm ultrastructure among logenetic analyses resulting from the relatively conserved closely related species. anuran bauplan (Inger 1967). Recently, analyses based on One of the best-studied groups of Anurans is the family other data sets such as mitochondrial DNA sequences have Hylidae, which consists of four subfamilies: Hemiphr- been profitably used in anuran phylogenetic reconstructions actinae, Hylinae (including pseudines, sensu Darst and (Hay et al. 1995; Darst and Cannatella 2004). The use of Cannatella 2004), Pelodryadinae and Phyllomedusinae. The © 2005 The Royal Swedish Academy of Sciences Sperm ultrastructure of Phyllomedusa • Costa et al. Acta Zoologica (Stockholm) 85: 257–262 (October 2004) most detailed works were on Australian hylids (Pelodryadi- nae) of the genera Litoria and Cyclorana (Lee and Jamieson 1993; Meyer et al. 1997; Scheltinga et al. 2002b). Few studies were made on Neotropical genera, including Pachymedusa (Rastogi et al. 1988) and Hyla (Pugin-Rios and Garrido 1981; Costa et al. 2004). These studies revealed several com- mon features of the hylid sperm as well as major differences, both among anuran families and within hylid genera. The genus Phyllomedusa (Phyllomedusinae) currently comprises 30 species ranging from Costa Rica to Argentina. There are few studies on the systematics and taxonomy of Phyllomedusa and not all species are assigned to species groups (Frost 2002). Herein, we provide detailed descrip- tions of sperm ultrastructure of Phyllomedusa hypochondrialis, Phyllomedusa bicolor, and Phyllomedusa tarsius, as well as a discussion on the variation of these characters within hylid genera and the use of sperm ultrastructure in systematics. Materials and methods We obtained spermatozoa from reproductive adult individu- als of the following species: Phyllomedusa hypochondrialis (CHUNB 14001–2, 24067), collected at Luziânia, Goiás Fig. 1—Schematic reconstruction of the spermatozoon of Phyllomedusa. State, Brazil (16°25′S, 47°95′W), and at Minaçu, Goiás State (13°38′S, 048°15′W); P. bicolor (CHUNB 22046) and regions: head (acrosome complex and nucleus), midpiece, P. tarsius (CHUNB 22047) collected near Manaus, Brazil and tail. The head is slightly curved, and the tail presents an (02°04′S, 060°03′W). We deposited vouchers at the ‘Coleção axial rod and an undulating membrane (Figs 2H and 3G). Herpetológica da Universidade de Brasília’ (CHUNB). Total sperm length was 60.62 µm ± 5.12 µm (n = 13) for P. We euthanized frogs by rubbing xylocaine 5% on the hypochondrialis, 81.60 µm ± 6.02 µm (n = 10) for P. bicolor, abdominal skin, removed testes and placed them in a Petri and 85.54 µm ± 4.48 µm (n = 13) for P. tarsius. Sperm dish with phosphate buffer (PBS) pH 7.2, and cut them into length differed significantly among species (; F = small pieces. We fixed tissues in a solution containing 85.28; P < 0.0001). Tukey’s multiple comparison tests 2.5% glutaraldehyde, 5 m CaCl2, and 5% sucrose in 0.1 indicated that sperm of P. h ypochondrialis is shorter than sodium cacodylate buffer pH 7.2 at 4 °C overnight, postfixed P. bicolor and P. tarsius, while differences between P. bicolor for 1 h in 1% osmium tetroxide, 0.8% potassium ferricya- and P. tarsius were not significant. nide, and 5 m CaCl2 in 0.1 sodium cacodylate buffer, pH 7.2. We dehydrated the material in a series of ascending Transmission electronic microscopy acetone (30–100%) and embedded tissues in Spurr’s epoxy resin. We stained ultra thin sections with uranyl acetate and The general structure of the sperm of Phyllomedusa is sche- lead citrate and made observations and photographed the matically shown in Fig. 1. The sperm ultrastructure of the material in a JEOL® 100C transmission electron micro- three species is similar and we therefore describe them scope. We made light microscopic observations of sper- together and indicate any differences. matozoa from 0.1 sodium cacodylate buffer pH 7.2 fixed smears under Normarsky contrast using a Zeiss® Axiophot Acrosome complex and nucleus microscope. We carried out statistical analyses using version 10.2 for Windows with a significance level of 5% to The acrosome complex (acrosome vesicle and subacrosomal reject null hypotheses. Throughout the text, means are cone) is located at the anterior region of the head and covers followed by one standard deviation (SD). the anterior part of the nucleus. The acrosome vesicle covers the subacrosomal cone and consists of a single, narrow vesi- cle filled with homogeneous material of low electron-density Results (Figs 2A–D and 3A–C). The subacrosomal cone lies under the acrosome vesicle forming a conical cap (Figs 2A–D and Light microscopy 3A–C). The acrosome vesicle goes from the tip of the cell to The spermatozoa of the three species of Phyllomedusa are the anterior region of the nucleus, whereas the subacrosomal elongate and filiform, consisting of three conspicuous cone goes beyond (Figs 2A, 2E, 3A,D). The acrosome vesicle © 2005 The Royal Swedish Academy of Sciences Acta Zoologica (Stockholm) 85: 257–262 (October 2004) Costa et al. • Sperm ultrastructure of Phyllomedusa and the subacrosomal cone are conical in longitudinal Discussion section (Figs 2A and 3A) and circular in cross sections (Figs 2B–E and 3B–D). The subacrosomal cone of P. bicolor The ultrastructure of the spermatozoa of the three species of and P. tarsius is more granular and less electron-dense in Phyllomedusa is similar. The major differences are in the transverse sections and striated in longitudinal sections, acrosome and tail regions. The spermatozoa of P. bicolor and relative to P. hypochondrialis (Figs 2A–E and 3A–D). P. tarsius are also significantly larger than that of P. h ypo- A well-defined electron lucent region, the nuclear space, lies chondrialis. Usually, sperm ultrastructure is conservative between the subacrosomal cone and the nucleus (Figs 2A, at the intrageneric level, but other studies also reported 2C–D and 3A). This space may be formed in the process of intrageneric variation, for example in Litoria (Lee and Jamieson chromatin condensation, during the spermiogenesis (Báo 1993; Meyer et al. 1997) and Pseudis (Garda et al.
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