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Descriptions of the Mature Spermatozoa of the Lizards

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Descriptions of the Mature Spermatozoa of the Lizards JOURNAL OF MORPHOLOGY 247:160–171 (2001) Descriptions of the Mature Spermatozoa of the Lizards Crotaphytus bicinctores, Gambelia wislizenii (Crotaphytidae), and Anolis carolinensis (Polychrotidae) (Reptilia, Squamata, Iguania) D.M. Scheltinga,1* B.G.M. Jamieson,1 R.E. Espinoza,2 and K.S. Orrell3 1Department of Zoology and Entomology, University of Queensland, Brisbane, Queensland, Australia 2Ecology, Evolution, and Conservation Biology, University of Nevada, Reno, Nevada 3Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia ABSTRACT The spermatozoa of Crotaphytus bicinctores similar to those of the agamids and phrynosomatids ex- and Gambelia wislizenii (Crotaphytidae), and Anolis caro- amined to date. No spermatozoal autapomorphies for Cro- linensis (Polychrotidae) exhibit the squamate autapomor- taphytidae or Polychrotidae were found. The condition of phies of a single perforatorium extending anteriorly from having the intermitochondrial dense bodies arranged in the apical tip of the paracrystalline subacrosomal cone, regular incomplete rings is tentatively defined as a syna- the presence of an epinuclear electron-lucent region, and pomorphy of Iguania (although modified in Chamaele- extension of the fibrous sheath into the midpiece. Crota- onidae). Spermatozoal ultrastructure offers no characters phytid sperm differ from those of polychrotids in several that justify the separation of Iguanidae (sensu lato) into respects, including: the structure of the perforatorium, the several separate families. J. Morphol. 247:160–171, 2001. size of the epinuclear electron-lucent region, aspects of the © 2001 Wiley-Liss, Inc. acrosome complex, the arrangement and structure of in- termitochondrial dense bodies, and in the distance the fibrous sheath extends into the midpiece. The sperm of C. KEY WORDS: Crotaphytus; Gambelia; Crotaphytidae; bicinctores, G. wislizenii, and A. carolinensis are most Anolis; Polychrotidae; Iguania; spermatozoa; phylogeny Sperm ultrastructure has been shown to provide tus (Furieri, 1974), although of questionable matu- valuable characters for phylogenetic studies (Jamie- rity, and in Polychrus acutirostris (Teixeira et al., son, 1995, 1999; Oliver et al., 1996; Teixeira et al., 1999a). Spermiogenesis has been examined in Ano- 1999b). As part of a larger study using sperm mor- lis carolinensis by Clark (1967). Here we describe phology in phylogenetic reconstructions of squamate the mature spermatozoon of A. carolinensis and reptiles, we provide the first description of the ma- compare it with that of other polychrotids, in partic- ture spermatozoon of three species of iguanian liz- ular that of P. acutirostris. ards representing two major clades: Crotaphytidae (Crotaphytus and Gambelia) and Polychrotidae (Anolis). Despite the lack of consensus and resolu- MATERIALS AND METHODS tion among the major clades of iguanian lizards Two male Crotaphytus bicinctores (UNR 6194-95), (Frost and Etheridge, 1989; Macey et al., 1997; were collected from Washoe Co., Nevada, USA, on 29 Schulte et al., 1998), monophyly of North American June 1998, and two male Gambelia wislizenii (UNR collared and leopard lizards (Crotaphytidae) has 7186-87) were taken from Mineral Co., Nevada, never been questioned (McGuire, 1996). Currently, USA, on 7 June 1999. Two male Anolis carolinensis Crotaphytidae contains two genera, Crotaphytus were collected from Augusta, Georgia, USA, on 7 and Gambelia, that have nine and three extant spe- November 1998. All lizards were in a reproductive cies, respectively (McGuire, 1996). While many as- state and were killed shortly after capture with a pects of the reproductive biology of crotaphytid liz- lethal injection of anesthetic. The testis and ducts ards have been well studied (reviewed in McGuire, were removed and fixed for TEM in 3% glutaralde- 1996), the morphology of crotaphytid sperm has not hyde in 0.1 M sodium phosphate buffer (pH 7.2) at been previously described. Here we provide detailed descriptions of the sperm of Crotaphytus bicinctores and Gambelia wislizenii. *Correspondence to David Scheltinga, Department of Zoology and Within Polychrotidae, mature spermatozoa have Entomology, University of Queensland, Brisbane, Australia, 4072. been previously described in Pristidactylus scapula- E-mail: [email protected] © 2001 WILEY-LISS, INC. Figure 1 162 D.M. SCHELTINGA ET AL. TABLE 1. Dimensions of spermatozoa taken from light and transmission electron microscopy Dimensions Crotaphytus bicinctores Gambelia wislizenii Anolis carolinensis Total length 85.5␮m(nϭ 32, SD ϭ 11.6) 98.8␮m(nϭ 19, SD ϭ 4.0) 83.2␮m(nϭ 32, SD ϭ 2.3) Head (acrosome and nucleus) 20.0␮m(nϭ 33, SD ϭ 0.06) 20.2␮m(nϭ 35, SD ϭ 0.9) 16.5␮m(nϭ 6, SD ϭ 0.2) Acrosome complex 4.73␮m(nϭ 8, SD ϭ 0.18) 4.74␮m(nϭ 3, SD ϭ 0.12) 5.76␮m(nϭ 6, SD ϭ 0.07) Nuclear rostrum 2.78␮m(nϭ 7, SD ϭ 0.11) 2.6␮m(nϭ 6, SD ϭ 0.13) 3.27␮m(nϭ 2, SD ϭ 0.09) Midpiece 3.99␮m(nϭ 9, SD ϭ 0.21) 4.97␮m(nϭ 8, SD ϭ 0.2) 4.61␮m(nϭ 15, SD ϭ 0.24) Tail 57.2␮m(nϭ 18, SD ϭ 11.8) 76.8␮m(nϭ 14, SD ϭ 4.6) 63.3␮m(nϭ 8, SD ϭ 2.6) Nuclear diameter (shoulders) 0.49␮m(nϭ 7, SD ϭ 0.03) 0.53␮m(nϭ 4, SD ϭ 0.02) 0.5␮m(nϭ 3, SD ϭ 0.03) Nuclear diameter (posterior) 0.67␮m(nϭ 9, SD ϭ 0.03) 0.68␮m(nϭ 6, SD ϭ 0.03) 0.65␮m(nϭ 9, SD ϭ 0.05) 4°C for at least 2 h before being transported at 3J, 5M). Dimensions of the sperm are provided in ambient temperature to Brisbane, Australia, for Table 1. processing and sectioning. The material was then rinsed in 0.1 M phosphate buffer, postfixed for 80 Acrosome Complex min in similarly buffered 1% osmium tetroxide, rinsed in buffer, dehydrated through an ascending The head (acrosome complex and nucleus) is long ethanol series (20–100%), and infiltrated and em- and curved. In longitudinal section the acrosome bedded in Spurr’s epoxy resin. complex appears sharply attenuated in one plane Sections were cut with diamond knives on a LKB (Figs. 1J,K, 5J,K) but flattened and spatulate in the 2128 UM IV microtome. Thin sections, 50–80 nm plane at right angles to this (Figs. 1A,B, 3A,I). Pos- thick, were collected on carbon-stabilized, colloidin- teriorly, the acrosome vesicle forms a progressively coated, 200 ␮m mesh copper grids, stained for 30 sec in narrowing sheath around the subacrosomal cone Reynolds’ lead citrate, rinsed in distilled water, then (Figs. 1B,J, 3A,I, 5K,L) and anteriorly can be divided placed in 6% aqueous uranyl acetate for 4 min, rinsed into a central medulla and surrounding cortex on in distilled water, and stained for a further 2 min in the basis of differences in electron density (Figs. lead citrate before final rinsing. Electron micrographs 1C–E, 3C, 5B–D,J). Cross striations are seen where were taken on a Hitachi 300 electron microscope at 75 the cortex and medulla join (Figs. 1E, 3C, 5B–D). kV. Light microscopic observations and photographs Within the acrosomal medulla, the subacrosomal of spermatozoa, from glutaraldehyde-fixed tissue space contains a perforatorium in the form of a very squashes, were made using an Olympus BH2 micro- narrow elongate cone with a pointed tip in Crota- scope with Nomarski interference contrast and an phytus bicinctores and Gambelia wislizenii (Figs. attached OM-2 camera. All spermatozoa described 1J,K, 3A,I), or a rounded tip in Anolis carolinensis and shown herein are from duct material. (Fig. 5J,K). When viewed in longitudinal section the perforatorium of A. carolinensis has distinct regular RESULTS transverse striations (Fig. 5J,K), whereas in C. bicinctores and G. wislizenii indistinct longitudinal The general structure of the spermatozoa of Cro- fibers are observed (Figs. 1A,B,J,K, 3A,I). The per- taphytus bicinctores, Gambelia wislizenii, and Ano- foratorium of all three species is in the same longi- lis carolinensis are sufficiently similar to be de- tudinal axis as the nuclear rostrum and at the apical scribed together, while noting the few observed tip of the subacrosomal cone has a slightly widened differences. The spermatozoa are filiform (Figs. 1L, basal modification, which is identifiable as a stopper-like perforatorial base plate (Figs. 1A,B,K, 3A,I, 5J,K). The material of the subacrosomal cone is Fig. 1 (Overleaf.) Crotaphytus bicinctores spermatozoon. A,B: paracrystalline. Within the anterior portion of the Longitudinal sections (L.Ss) through the nuclear rostrum and cone, anterior to the nuclear rostrum, an epinuclear acrosome. Note the stopper-like perforatorial base plate. C–H: A series of transverse sections (T.Ss) through the acrosome and electron-lucent region is present in all three species. nucleus. Note that anteriorly in C–F the acrosome is laterally In Crotaphytus bicinctores and Gambelia wislizenii compressed in transverse section, while further posteriorly, in G, this region is large and well developed (Figs. it is unilaterally ridged, and at its posterior limit, in H, it is 1A,B,F,J, 3A,I), whereas in Anolis carolinensis it is circular. I: T.S. through the nucleus. J,K: L.Ss through the acro- small but still distinct (Fig. 5E,J). some showing the concentric zonation of the acrosome vesicle and the epinuclear electron-lucent region. L: Whole spermatozoon At the base of the nuclear rostrum the acrosome (Nomarski contrast light microscopy). A–K to the same scale as complex is circular in transverse section (Figs. 1H, indicated. av, acrosome vesicle; cd, cytoplasmic droplet; co, cortex 3G). In the direction of the tip of the acrosome ves- of acrosome vesicle; et, epinuclear electron-lucent region; h, icle the acrosome complex becomes progressively de- sperm head (acrosome and nucleus); me, medulla of acrosome vesicle; mp, midpiece; n, nucleus; nr, nuclear rostrum; ns, nuclear pressed (Figs.
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