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Sperm Morphology and Spermiogenesis in the Methane-Seep Mollusc Bathynerita Naticoidea (Gastropoda: Neritacea) from the Louisiana Slope

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Sperm Morphology and Spermiogenesis in the Methane-Seep Mollusc Bathynerita Naticoidea (Gastropoda: Neritacea) from the Louisiana Slope FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1998 American Microscopical Society. This manuscript is an author version with the final publication available at http://www.wiley.com/WileyCDA/ and may be cited as: Hodgson, A. N., Eckelbarger, K. J., & Young, C. M. (1998). Sperm morphology and spermiogenesis in the methane‐seep mollusc Bathynerita naticoidea (Gastropoda: Neritacea) from the Louisiana slope. Invertebrate Biology, 117(3), 199‐207. " ~7., } Invertebrate Biology J 17(3): 199-207. \ © 1998 American Microscopical Society. Inc. Sperm morphology and spermiogenesis in the methane-seep mollusc Bathynerita naticoidea (Gastropoda: Neritacea) from the Louisiana slope Alan N. HodgsonY Kevin J. Eckelbarger,2 and Craig M. Young3 .. IOepartment of Zoology & Entomology. Rhodes University, Grahamslown 6140, South Africa 20arling Marine Centre, University of Maine, Walpole, Maine 04573, USA and School of Marine Sciences, University of Maine, Orono, Maine 04469, USA JDivision of Marine Sciences, Harbour Branch Oceanographic Institution, Fort Pierce, FL 34946, USA Abstract. Bathynerita nalicoidea, a bathyal neritid prosobranch endemic to oil and gas seeps in the Gulf of Mexico, produces filiform eusperms ~90 J.Lm long. The euspeffil is of the introspeffil type, typical of invertebrates with internal fertilization, and they are similar in structure to those of shallow-water neritimorph taxa. The head of the sperm is ~26 J.Lm long and consists of an elongate tubular nucleus (-24 J.Lm long X 0.2 J.Lm diameter) and acrosome (~2 J.Lm long), which sits on a subacrosomal plate. The anteriorly positioned acrosome is invaginated posteriorly, with the subacrosomal space containing an axial rod. The mid-piece, which is -35 J.Lm long, contains two elongate mitochondria, housed in a cytoplasmic sheath, the inner membrane of which is periodically thickened. The centriolar complex is housed in the intra-nuclear canal, 1 J.Lm from the anterior of the nucleus. Thus the axoneme penetrates most of the length of the nucleus. Associated with the first outer doublets of the axoneme is a rod-like structure which runs the length of the mid-piece and for part of the tail. Unlike most other neritids, the axoneme of B. naticoidea is not bent at the junction of the mid-piece and tailpiece, and the tail is not terminally expanded. Whilst the sperm of B. naticoidea has many structural similarities to those of other Neritidae, the simple terminal end and more elongate mid-piece rod suggests that Bathynerita may be more closely related to the Phenacolepadidae than the Neritidae. Spermiogenesis is as described for shallow water neritids. Associated with the developing speffilatids are Sertoli cells, the structure of which is similar to that described for other gastro­ pods. Additional key words: prosobranch, deep-sea, eusperm, introsperm, Sertoli cell The Neritacea are prosobranch gastropods common­ tribution, being particularly well adapted to the high ly found in subtropical and tropical aquatic habitats shore. However, a number of deep-sea species have (Fretter 1965) as well as some terrestrial habitats been discovered recently (Haszprunar 1988; Waren & (Knight et a1. 1960). The superfamily contains 6 extant Bouchet 1993), but their relationship to shallow water families; Neritidae, Neritopsidae, Phenacolepadidae, taxa has still to be established. One such deep-sea ner­ Titiscaniidae, Hydrocenidae and Helicinidae. Relation­ itid, Bathynerita naticoidea CLARK 1989 (Neritidae), is ships within the Neritacea, and between this and other endemic to oil and gas seeps in the northern Gulf of prosobranch taxa, are far from clear. The neritids are Mexico continental slope (Clarke 1989). regarded, however, as an early offshoot of the gastro­ Studies on speffil ultrastructure and spermiogenesis pods (Haszprunar 1988; Healy 1996) and most phy­ have provided valuable insights into taxonomic and logenies place them towards the base of prosobranch phylogenetic relationships of many invertebrate taxa phylogenetic trees (Haszprunar 1988; Ponder & Lind­ (Jamieson et al. 1995). In addition the structure of berg 1996; Ponder & Lindberg 1997). speffils can be used to determine the environment of Most marine neritimorphs are intertidal in their dis- fertilization (i.e. external or internal fertilization) (Franzen 1956; Jamieson 1987). To date the only de­ scriptions of neritimorph speffil morphology and sper­ • Author for correspondence. miogenesis are from shallow water species (Nishiwaki E-mail: [email protected] ] 964; Garreau de Loubresse 1971; Giusti & Selmi 200 Hodgson, Ecklebarger, & Young ditional two males were collected in August 1997 from Bush Hill (27°47'N, 91° 30.4'E) in the GlllfofMexico in 540 m of water. These specimens were preserved in 4% formalin and subsequently transferred to 70% al­ cohol for light microscopy. • I For light microscopy small portions of the gonad n and vas deferens were smeared onto a microscope slide and air dried. Twenty sperm were measured from each of the two males using a Nikon filar micrometer eyepiece. Sperm were also photographed using an Olympus BX photomicroscope. For transmission electron microscopy, smal1 por­ tions of the testis were immersed for 1.5 h (4°C) in a mp' primary fixative containing 3% glutaraldehyde, 1% ,, formaldehyde made from paraformaldehye, 0.1 M Mil­ lonig's phosphate buffer (pH 7.4), 3% NaCI and 3.5% sucrose. The tissue was then rinsed for 30 min in three changes of cold (4°C) 0.1M Millonig's phosphate buff­ er containing 6% sucrose. The tissue was then post­ fixed for 1.5 hours at room temperature in 1% OS04 in 0.1 M Millonig's phosphate buffer and dehydrated for 2 hours in ascending concentrations of ethanol to .. 100%. Tissues were embedded in Epon via propylene oxide. Semi-thin and ultra-thin (silver/gold interface) sections were cut on an RMC7 ultramicrotome, and \ stained in 1% toluidine blue (in 2.5% sodium carbon­ Fig. 1. Light micrograph of a eusperm of Bathynerita na­ ate) or 5% aqueous uranyl acetate (20 min) and lead ticoidea. a, acrosome; mp, mid-piece; n, nucleus; t, tail. citrate (3 min) respectively. Sections were viewed on Scale bar= 10 fJ-m. a JEOL 100CXII TEM at 80kv. Results 1982; Selmi & Giusti 1983a, b; Kohnert & Storch 1984; Koike 1985; Buckland-Nicks & Chia 1986a; AI­ Despite being sampled from depth, the fixation of Hajj 1988). Healy (1996) has suggested that investi­ tissues and preservation of cell detail were remarkably gations of species which inhabit hydrothermal vents good. and seeps will provide a greater understanding of gas­ tropod evolution; deep-sea fauna often being the Spenn morphology source of relict characters. In this paper we provide The testis of the individuals studied possessed eu­ the first description of the sperm and spermiogenesis sperms which are of the introsperm type (Rouse & of a deep-sea neritid, B. naticoidea, and comment on Jamieson 1987) and typical of animals with internal the possible relationship of this bathyal species to its fertilization (Jamieson 1987). shallow water relatives. This paper complements the The ellsperm, which is ~90 J.Lm long, is filiform in recent paper in which the ultrastructure of the ovary shape with a long, thin head (~26 J.Lm long and 0.6 and oogenesis was described (Eckelbarger & Young J.Lm diameter) (Fig. I), mid-piece and tai1. The head 1997). has an elongate nucleus (~24 J.Lm long) which is pen­ etrated for its entire length by an intra-nuclear canal Methods (-0.2 J.Lm diameter) (Figs. I; 2a, b). The nucleus is Live specimens of Bathynerita naticoidea were col­ capped by an acrosome which is -2 J.Lm long and lected in September 1995 by the Johnson-Sea-Link II deeply invaginated posteriorly (Fig. 2b). The posterior submersible at Green Canyon block 232 ("brine third of the acrosome is cylindrical in shape (~0.2 fJ-m pool") in 710 m of water (2r 43.327'N, 91° diameter), whereas the anterior two thirds is narrower 16.606'W), in the Gulf of Mexico. Amongst the spec­ (~O.l J.Lm diameter). The subacrosomal space contains imens a single male was found and tissues from it were an axial rod which is expanded posteriorly as a cone­ prepared for transmission electron microscopy. An ad- shaped structure (Fig. 2b, d). Between the base of the ... .; , -'~.' . ~ ~ ".' ..~~~:- :'~ _.:>:" . Bathynerita sperm structure 201 Fig. 2. Transverse and longitudinal sections through the eusperm of Bathynerita naticoidea. a. Longitudinal section of the head. b. Longitudinal section of the acrosome showing the posterior expansion of the axial rod (arrowed). c. Base of the acrosome and subacrosomal plate (sa). d. Transverse sections through various regions of the acrosome. e. Transverse section though the nucleus and centriole (c) within the intra nuclear canal. f. Longitudinal section of the anterior nucleus showing centriole (c) within the intra nuclear canal. g, h. Longitudinal sections of the mid-piece showing axoneme and mid-piece rod (r) surrounded by mitochondria (m) in the cytoplasmic sheath. Note the periodic electron-dense thickening of the sheath membrane (aITowed). i. Transverse sections of the mid-piece and tail. j. Longitudinal section of the junction between the mid-piece and tail. k. Longitudinal section of the terminal region of the tail. a, acrosome: ar, axial rod; ax, axoneme; c, centriole: gl, glycogen: i, intra nuclear canal; n, nucleus; r, mid-piece rod: sa, subacrosomal r1ate: t, tad; tr, terminal region of tail. Scale bars; a=2 I-lm; b, f-k=O.5 I-lm; c,d,e=O.25 I-lm. 202 Hodgson, Ecklebarger, & Young acrosome and the anterior of the nucleus is a subacro­ large mitochondria (~l J.Lm diameter) with well de­ somal plate which is perforated centrally (Fig. 2c). veloped tubular cristae (Fig. 3b, c; 4a). The cytoplas­ The mid-piece consists of a centriolar complex mic extensions often contain microfiJaments (Fig.
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