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FAU Institutional Repository FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: ©1989 Marine Biological Laboratory. The final published version of this manuscript is available at http://www.biolbull.org/. This article may be cited as: Eckelbarger, K. J., Young, C. M., & Cameron, J. L. (1989). Ultrastructure and Development of Dimorphic Sperm in the Abyssal Echinoid Phrissocystis multispina (Echinodermata: Echinoidea): Implications for Deep Sea Reproductive Biology. The Biological Bulletin, 176(3), 257‐271. Reference: BioL Bull. 176: 257—271.(June, 1989) Ultrastructure and Development of Dimorphic Sperm in the Abyssal Echinoid Phrissocystis multispina (Echinodermata: Echinoidea): Implications for Deep Sea Reproductive Biology KEVIN J. ECKELBARGER, CRAIG M. YOUNG, AND J. LANE CAMERON Division ofMarine Sciences, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Fort Pierce, Florida 34946 Abstract. Mature males of the abyssal echinoid Phris et a!., 1982; Tyler, 1988). Until now, however, technol socystis multispina produce two types of sperm includ ogy has restricted the study of deep-sea reproduction ing a euspermatozoon typical of echinoids, and a para largely to the analysis of paraffin sections of preserved spermatozoon, which is bipolar-tailed. The structure of gonads collected from trawls or dredge collections the testis and most features of spermatogenesis are sim (Georgeand Menzies1967,1968;Rokop, 1974,1977; ilar to that of other echinoids. Development of both Ahfeld, 1977; Pain et a!., 1982a, b; Tyler and Gage, 1982, sperm types is identical until the spermatid stage when 1983, 1984; Tyler et al., 1982). Little is known about ga the nucleus ofthe paraspermatozoon undergoes chroma mete structure, fertilization biology, or development of tin reduction. Both sperm types have acrosomes typical any deep-sea species due, in part, to the difficulty of oh ofother echinoid sperm. However, we never observed a taming live specimens in good condition. Golgi complex during any stage ofsperm differentiation Echinoderm sperm have been extensively studied and, so the origin of the acrosome is unclear. Both the distal in comparison to most invertebrate sperm, are morpho and proximal centrioles are involved in the formation logically conservative (Chia and Bickell, 1983). This ofan anteriorly and posteriorly directed flagellum in the study describes the ultrastructural features of spermato paraspermatozoon. Mixtures of both sperm types tend genesis in Phrissocystic multispina, a deep-sea spatan to clump due to the entanglement ofsperm axonemes in goid collected in Hawaiian waters with the Pisces V suh the paraspermatozoon flagellum. Although the function mersible. Males ofP. multispina have dimorphic sperm, ofthe paraspermatozoa is unknown, they may play a role the first recorded occurrence in the Echinodermata, and in facilitating fertilization through the reduction of eu although one type of sperm is typical of echinoids, the spermatozoon diffusion during spawning. This study re other is bipolar-tailed, a feature which is structurally rare ports only one of several recently discovered reproduc among metazoan sperm. tive adaptations associated with deep-sea habitats. Animal sperm morphology is strongly influenced by the mode offertilization and the environment into which Introduction the sperm are released during spawning (Franzen, 1956, Echinoderms are often the most abundant and diverse 1970). The appearance ofdimorphic, aberrant sperm in macrofaunal organisms in the abyssal and bathyal zones P. multispina and unusual sperm in several other deep of the ocean (Billet and Hansen, 1982; Pawson, 1982) sea echinoderms (Healy et al., 1988; Eckelbarger et a!., and the reproductive cycles of many deep-sea species in press) suggests that unique selective pressures may be have been investigated (see Lightfoot et a!., 1979; Tyler present in the abyssal zone ofthe deep sea which are ah sent from shallow water habitats. The present paper de scribes the ultrastructural features ofspermatogenesis in Received 25 January 1989; accepted 3 April 1989. this species and discusses the potential factors influenc 257 258 K. J. ECKELBARGERET AL. @ 1@' •¿@-‘¿ .@‘¿ , •¿ I *‘ @ ,. @ @,T--@ cm -_@. @S 1 2 ,@ . @. @ ‘¿@:¼@@:‘. @ @. -‘;. s;.; •¿@‘¿ @ .:@: DIMORPHIC SPERM OF ABYSSAL ECHINOID 259 ing the evolution ofthese unusual gametes. This investi lacral plates in the apical halfofthe perivisceral coelom. gation represents only the third study of gamete ultra A cross section through a single acinus of the testis re structure in a deep-sea organism. The ultrastructure of veals a thin, apparently unflagellated outer perivisceral sperm development in the vestimentiferan, Riflia pa epithelium, followed by a thick (3.5—4 @m)collagenous chyptila, was previously described from specimens col connective tissue layer, a narrow perihemal sinus lined lected near hydrothermal vent communities using the by a thin basal lamina and containing prominent muscle manned submersible Alvin (Gardiner and Jones, 1985). cells, a hemal sinus about 2 @imin width, and the testis Recently, aberrant sperm were reported in Xyloplax, a lumen lined by a germinal epithelium (Fig. 4). The he deep sea representative of the new echinoderm class, mal sinus periodically evaginates into the testis lumen Concentricycloidea (Healy et a!., 1988). creating columns of developing sperm cells (Fig. 2). Elongated interstitial cells (Fig. 3) are often observed in Materials and Methods association with developing germ cells and contain a va Six live, sexually mature specimens of Phrissocystis riety ofspherical electron-dense granules and numerous, multispina (four male and two female) were collected off parallel microtubules arranged in the long axis ofthe cell Kailua-Kona, Hawaii, in July 1988 at depths ranging (Fig.3,insert). from 875 m to 1920 m using the Pisces V submersible (Fig. 1). Specimens were dissected on board ship shortly Spermatogonia and spermatocytes after collection and testes were removed for immediate We observed two morphological types ofsperm in four fixation. Whole testes were fixed for 1h in a primary fix male specimens of Phrissocystis muhispina. The two ative (2.5% glutaraldehyde in 0.2 M sodium cacodylate, types appear in approximately equal proportions, based 0.1 MNaC1, and 0.35 Msucrose at 4°C)and then washed on squashes offresh testes and examination of histologi in three changes of 0.2 M sodium cacodylate, 0.3 M cal sections. Due to extensive injury to specimens during NaC1, and 0.35 M sucrose. Tissue was then postfixed in submersible collection, we were unable to observe 1%0504 in 0.2 M sodium cacodylate, 0.3 M NaCl, and spawning in intact animals. One spermatozoan type is 0.35 M sucrose at room temperature. Tissues were then “¿typical―for echinoids while the second is bipolar-tailed dehydrated in ascending concentrations of ethanol, and “¿atypical―in morphology. Limited observations of transferred through two changes ofpropylene oxide, and living sperm indicated that both types were motile but embedded in Epon. Thick sections were cut on a Porter sluggish swimmers. Various terms have been suggested Blum MT2-B ultramicrotome using a diamond knife, to describe polymorphic sperm based on differences in mounted on slides, stained with Richardson's stain, and nuclear chromatin (Meves, 1903; Melone et a!., 1980; photographed with a Zeiss WL research compound mi Buckland-Nicks et a!., 1982). However, the two types of croscope. Thin sections were cut with a diamond knife sperm observed in P. muhispina appear to have identical and stained with alcoholic saturated uranyl acetate and nuclear morphology. To avoid the proliferation of new aqueous lead citrate for 10 mm each, then examined in terminology, we have adopted the terms “¿euspermato a Zeiss EM9S-2 transmission electron microscope. zoon―for the typical sperm and “¿paraspermatozoon― Dried specimens of Phrissocystis multispina have (para: near, close) for the atypical sperm as proposed by been deposited with the U. S. National Museum, Smith Healy and Jamieson (198 1). Differentiation of these sonian Institution (USNM # E 37821). sperm cannot be distinguished until the early spermatid Results stage so earlier development will be described for both simultaneously. Spermiogenesis will be described sepa Structure ofthe testis wall rately for each sperm type. The testes are arborescent structures suspended by Examination of the germinal epithelium reveals the folds ofthe perivisceral epithelium from the interambu presence ofspermatogonia and spermatocytes, while the Figure 1. Adult specimen ofPhrissocystis multispina photographed from the Pisces V submersible at a depth of 1920 m offKailua-Kona, Hawaii. Figure 2. Light microscopic transverse section through the testis wall. Arrows indicate invagination of hemal sinus into testis lumen. C, coelom; SP, sperm cells; W, wall of testis. Figure 3. Interstitial cell(IS) containing electron dense inclusions(°)surrounded by developing sperm cells(SP). Insert: higher magnification ofinterstitial cellcytoplasm showing parallelarrays of microtubules. Figure4. Transversesection throughthe testis wall showing the outer coelomic peritoneum (CP);con nective tissue layer (CT); large muscles cells (M) within the perihemal sinus (PHS); the hemal sinus (HS) lined by a basal lamina (BL) and adjacent to a germinal epithelium containing spermatogonia (SPO) and spermatocytes(SPC).
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