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Spermatogenesis, sperm storage and comparative sperm morphology in nine species of Capitella, Capitomastus and Capitellides (Polychaeta: Capitellidae)

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Abstract

Light microscopy and transmission electron microscopy (TEM) were used to describe spermatogenesis and the morphology of mature sperm and sperm storage organs in five sibling species of Capitella, three species in the related genus Capitomastus, and one species in the genus Capitellides. These capitellids lack a well-developed testis, but young males have a few specialized regions of the peritoneum in the eighth setiger, where germ cells proliferate and spermatogonia are released into the coelom, and spermiogenesis is completed. Mature sperm are stored in the central regions of paired genital ducts (coelomoducts), which lie between the seventh and eighth setigers. The cells forming the walls of the coelomostome and central region of the duct are ciliated and have large glycogen deposits. The lumenal borders have extensive microvilli and there is evidence that they secrete glycogen-containing materials into the duct. All species have modified primitive sperm with a conical acrosome, elongated nucleus, and long middle piece extending along the proximal portion of the flagellum. A single ring-shaped mitochondrion encircles the centriolar region of the middle piece and the cytoplasm is filled with glycogen. The sperm of all nine species differ significantly in the lengths of their middle pieces, acrosomes and especially in their nuclear lengths. The nuclear lengths have a twofold range among the sibling species of Capitella and Capitomastus. Subtle differences in the shape and volume of the acrosomal vesicle and acrosomal space characteristic of the Capitella sibling species seem to correlate with a basic division of these species into those with diploid chromosome numbers of 20 or 26. Spermiogenesis, the number of sperm produced, and the method of sperm storage are appropriate for efficient sperm utilization in fertilization. No evidence indicates that spermatophores are formed and transferred between individuals and the method of sperm transfer is not understood. The differences in the dimensions and acrosome morphology of mature sperm, and the previously demonstrated specializations in the egg envelopes in the Capitella sibling species, are characteristic features of the reproductive isolation that exists among these capitellid species.

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Literature cited

  • Afzelius, B. A.: Sperm structure in relation to phylogeny in lower metazoa. In: The Spermatozoon: maturation, motility, surface properties and comparative aspects, 441 pp. Ed. by D. W. Fawcett and J. M. Bedford. Baltimore: Urban & Schwarzenberg 1979

    Google Scholar 

  • Afzelius, B. A., and M. Ferraguti: Fine structure of brachiopod spermatozoa. J. Ultrastruct. Res. 63, 308–315 (1978)

    PubMed  Google Scholar 

  • Åkesson, B.: Incipient reproductive isolation between geographical populations of Ophryotrocha labronica (Polychaeta, Dorvilleidae) Zool. Scripta 1, 207–210 (1972)

    Google Scholar 

  • Åkesson, B.: Crossbreeding and geographic races: experiments with the polychaete genus Ophryotrocha. Mikrofauna Meeresboden 61, 1–18 (1977)

    Google Scholar 

  • Anderson, W. A. and W. R. Eckberg: A cytological analysis of fetilization in Chaetopterus pergamentaceous. Biol. Bull. mar. biol. Lab., Woods Hole 165, 110–118 (1983)

    Google Scholar 

  • Anderson, W. A. and P. Personne: The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. J. Cell. Biol. 44, 29–51 (1970)

    Article  PubMed  Google Scholar 

  • Arnaud, J.: Modifications ultrastructurales du chondriome durant la spermiogenèse chez Sagitta bipunctata Quoy et Gaiu. Bull. Soc. Zool. Fr. 93, 561–568 (1968)

    Google Scholar 

  • Atwood, D. G.: Fine structure of an elongated dorso-ventrally compressed echinoderm (Holothuroidea) spermatozoon. J. Morph. 145, 189–208 (1975)

    Google Scholar 

  • Bashor, D. P. and R. H. Quinn: Ultrastructure of the dorsal ciliated organ of Nereis virens: evidence of transepithelial transport. Trans. Am. Microsc. Soc. 100, 421–426 (1981)

    Google Scholar 

  • Bass, N. R. and A. E. Brafield: The life cycle of the polychaete Nereis virens. J. mar. biol. Ass. u.K. 52, 701–726 (1972)

    Google Scholar 

  • Bertout, M.: Spermatogenèse de Nereis diversicolor O. F. Müller (Annélide Polychète) 1. Évolution du cytoplasme et élaboration de l'acrosome. J. Microsc. Biol. Cell. 25, 87–94 (1976)

    Google Scholar 

  • Boletzky, S. v. and W. Dohle. Observations sur un capitellide (Capitella hermaphrodita sp. n.) et d'autres polychètes habitant la ponte de Loligo vulgaris. Vie Milieu Ser. Biol. Marin A 18, 79–98 (1967)

    Google Scholar 

  • Chia, F.-S. and L. R. Bickell: Echinodermata. In: Reproductive biology of invertebrates, vol. II, 692 pp. Spermatogenesis and sperm function. Ed. by K. G. Adiyodi and R. G. Adiyodi, New York: John Wiley & Sons 1983

    Google Scholar 

  • Christie, G.: The reproductive cycles of two species of Pholoe (Polychaeta: Sigalionidae) off the Northumberland coast. Sarsia 67, 283–292 (1982)

    Google Scholar 

  • Christie G.: A comparative study of the reproductive cycles of three Northumberland populations of Chaetozone setosa (Polychaeta: Cirratulidae). J. mar. biol. Ass. U.K. 65, 239–254 (1985)

    Google Scholar 

  • Clark, R. B. and P. J. W. Olive: Recent advances in polychaete endocrinology and reproductive biology. Oceanogr. mar. Biol. A. Rev. 11, 175–222 (1973)

    Google Scholar 

  • Clark, R. B.: Environmental determination of reproduction in polychaetes. In: Reproductive ecology of marine invertebrates. 283 pp. Ed. by S. E. Stancyk. Columbia: Univ. South Carolina Press 1979

    Google Scholar 

  • Daly, J. M. and D. W. Golding: A description of the spermatheca of Spirorbis spirorbis (L.) (Polychaeta: Serpulidae) and evidence for a novel mode of sperm transmission J. mar. biol. Ass. U.K. 57, 219–227 (1977)

    PubMed  Google Scholar 

  • Day, R. L. and J. A. Blake: Reproduction and larval development of Polydora giardi Mesnil (Polychaeta: Spionidae). Biol. Bull. mar. biol. Lab., Woods Hole 156, 20–30 (1979)

    Google Scholar 

  • Eckelbarger, K. J.: Ultrastructural evidence for both autosynthetic and heterosynthetic yolk formation in the oocytes of an annelid (Phragmatopoma lapidosa: Polychaeta). Tiss. Cell 11, 425–443 (1979)

    Article  Google Scholar 

  • Eckelbarger, K. J.: Ultrastructure of spermatogenesis in the reefbuilding polychaete Phragmatopoma lapidosa (Sabellariidae) with special reference to acrosome morphogenesis. J. ultrastruc. Res. 89, 146–164 (1984)

    Google Scholar 

  • Eckelbarger, K. J. and J. P. Grassle: Ultrastructural differences in the eggs and ovarian follicle cells of Capitella (Polychaeta) sibling species. Biol. Bull. mar. biol. Lab., Woods Hole 165, 379–393 (1983)

    Google Scholar 

  • Eckelbarger, K. J. and J. P. Grassle. Interspecific variation in genital spine, sperm and larval morphology in six sibling species of Capitella. Bull Biol. Soc. Wash. 7, 62–76 (1987)

    Google Scholar 

  • Eisig, H.: Die Segmentalorgane der Capitelliden. Mitt. zool. Stat. Neapel 1, 93–118 (1878)

    Google Scholar 

  • Eisig, H.: Die Capitelliden des Golfes von Neapel. Fauna Flora Golfes Neapel 16, 1–906 (1887)

    Google Scholar 

  • Fauchald, K.: The polychaete worms, 188 pp. Nat. Hist. Mus. Los Angeles County, Sci. Ser. 28, 1977

  • Fawcett, D. W., W. A. Anderson and D. M. Phillips: Morphogenetic factors influencing the shape of the sperm head. Devel. Biol. 26, 220–251 (1971)

    Google Scholar 

  • Ferraguti, M. and G. Lanzavecchia: Morphogenetic effects of microtubules. I. Spermiogenesis in Annelida Tubificidae. J. Submicrosc. Cytol. 3, 121–137 (1971)

    Google Scholar 

  • Franzén, A.: On spermiogenesis, morphology of the spermatozoan and biology of fertilization among invertebrates. Zool. Bidr. Fran Uppsala 31, 355–482 (1956)

    Google Scholar 

  • Franzén, A.: Phylogenetic aspects of the morphology of spermatozoa and spermiogenesis. 573 pp. In: Comparative spermatology. Ed. by B. Baccetti. New York: Academic Press 1970

    Google Scholar 

  • Franzén, A.: Sperm ultrastructure in some Polychaeta. In: The functional anatomy of the spermatozoon, pp 267–278. Ed. by B. A. Afzelius. New York: Pergamon Press 1975

    Google Scholar 

  • Franzén, A.: Ultrastructure of spermatids and spermatozoa in three polychaetes with modified biology of reproduction: Autolytus sp., Chitinopoma serrula, and Capitella capitata. Int. J. Invertebr. Reprod. 5, 185–200 (1982a)

    Google Scholar 

  • Franzén, A.: Ultrastructure of the biflagellate spermatozoon of Tomopteris helgolandica Greef, 1879 (Annelida, Polychaeta). Gamete Res. 6, 29–37 (1982b)

    Google Scholar 

  • Franzén, A.: Ultrastructural studies of spermatozoa in three bivalve species with notes on evolution of elongated sperm nucleus in primitive spermatozoa. Gamete Res. 7, 199–214 (1983)

    Google Scholar 

  • George, J. D.: The behaviour and life history of a mangrovedwelling capitellid (Polychaeta), pp 323–337. Proc. 1st int. Polychaete Conf., Sydney. Ed. by P. A. Hutchings. New South Wales: Linn Soc. 1984

    Google Scholar 

  • Gidholm, L.: On the morphology of the sexual stages, mating and egg-laying in Autolytus (Polychaeta). Zool. Bidr. Fran Uppsala 37, 1–44 (1965)

    Google Scholar 

  • Grassle, J. P.: Speciation in the genus Capitella (Polychaeta, Capitellidae). Fortschr. Zool. 29, 293–298 (1984)

    Google Scholar 

  • Grassle, J. P., C. E. Gelfman and S. W. Mills: Karyotypes of Capitella sibling species and of several species in the related genera Capitellides and Capitomastus (Polychaeta). Bull. Biol. Soc. Wash. 7, 77–88 (1987)

    Google Scholar 

  • Grassle, J. P. and J. F. Grassle: Sibling species in the marine pollution indicator Capitella (Polychaeta). Science, Wash. D.C. 192, 567–569 (1976)

    Google Scholar 

  • Grassle, J. P. and J. F. Grassle: The utility of studying the effects of pollutants on single species populations in benthos of mesocosm and coastal ecosystems, pp 621–642. In: Concepts in marine pollution measurements. Ed. by H. H. White, College Park, MD: Maryland Sea Grant Publication 1984

    Google Scholar 

  • Guérin, J.-P.: Redescription des adultes et comparaison des divers stades ontogénétiques des populations mediterranéennes et atlantiques de Scolelepis fuliginosa Claparède (Annélide Polychete). Cah. Biol. mar. 16, 21–37 (1975)

    Google Scholar 

  • Guérin, J.-P. and P. Kerambrun: Role of reproductive characters in the taxonomy of spinoids and elements of speciation in the “Malacoceros fuliginosus complex”. Fortsch. Zool. 29, 317–333 (1984)

    Google Scholar 

  • Hartman, O.: Polychaetous annelids. Pt. 7. Capitellidae. Allan Hancok Pacific Expeditions 10, 391–481 (1947)

    Google Scholar 

  • Hauenschild, C.: Nachweis der sogenannten atoken Geschlechtsform des polychaeten Platynereis dumerilii Aud. et M. Edw. als eigene Art auf Grund von Zuchtversuchen. Zool. Jb. Physiol. 63, 107–128 (1951)

    Google Scholar 

  • Holbrook, M. J. L. and J. P. Grassle: The effects of low density on the development of simultaneous hermaphroditism in male Capitella sp. I (Polychaeta). Biol. Bull. mar. biol. Lab., Woods Hole 166, 103–109 (1984)

    Google Scholar 

  • Holland, N. D.: Morphologically specialized sperm from the ovary of Isometra vivipara (Echinodermata-Crinoidea). Acta Zool. (Stockh). 57, 147–152 (1976)

    Google Scholar 

  • Huebner, E.: Spermathecal ultrastructure of the insect Rhodnius prolixus Stal. J. Morph. 166, 1–25 (1980)

    Google Scholar 

  • Jamieson, B. G. M.: Spermiogenesis in the oligochaetoid polychaete Questa (Annelida, Questidae). Zool. Scripta 12, 179–186 (1983)

    Google Scholar 

  • Jamieson, B. G. M., K. S. Richards, T. P. Fleming and C. Erseus: Comparative morphometrics of oligochaete spermatozoa and egg-acrosome correlation. Gamete Res. 8, 149–169 (1983)

    Google Scholar 

  • Kubo, M. and N. Sawada: Electron microscope study on sperm differentiation in Perinereis brevicirris (Polychaeta). Cell Struct. Funct. 2, 135–144 (1977)

    Google Scholar 

  • Longo, F. J. and E. Anderson: Sperm differentiation in the sea urchins Arbacia punctulata and Strogylocentrotus purpuratus. J. ultra struct. Res. 27, 486–509 (1968)

    Google Scholar 

  • Olive, P. J. W.: Annelida-Polychaeta. In: Reproductive biology of invertebrates, vol. II. 692 pp. Spermatogenesis and sperm function. Ed. by K. G. Adiyodi and R. G. Adiyodi. New York: John Wiley & Sons 1983

    Google Scholar 

  • Petraitis, P.: Females inhibit males' propensity to develop into simultaneous hermaphrodites in Capitella sp. I. (Polychaeta). Biol. Bull. mar. biol. Lab., Woods Hole 168, 395–402 (1985)

    Google Scholar 

  • Pfannensteel, H.-D. and C. Grunig: Gametogenesis and reproduction in nereid sibling species (Platynereis dumerilii, P. massiliensis) Am. Zool. 24, 43A (1984)

  • Potswald, H. E.: An electron microscope study of spermiogenesis in Spirorbis (Laeospira) morchi Levinsen (Polychaeta). Zeitschr. Zellforsch. 83, 231–248 (1967)

    Google Scholar 

  • Reish, D. J.: The establishment of laboratory colonies of polychaetous annelids. Thalassia jugosl. 10, 181–185 (1974)

    Google Scholar 

  • Rice, S. A.: Ultrastructure of the male nephridium and its role in spermatophore formation in spionid polychaetes (Annelida). Zoomorph. 95, 181–194 (1980)

    Google Scholar 

  • Rice, S. A.: Spermatogenesis and sperm ultrastructure in three species of Polydora and in Streblospio benedicti (Polychaeta: Spionidae). Zoomorph. 97 1–16 (1981)

    Google Scholar 

  • Rice, S. A. and J. L. Simon: Intraspecific variation in the pollution indicator polychaete Polydora ligni (Spionidae). Ophelia 19, 79–115 (1980)

    Google Scholar 

  • Rothchild, L. and K. W. Cleland: The physiology of sea urchin spermatozoa. The nature and localization of the endogenous substrate. J. exp. Biol. 29, 66–71 (1952)

    Google Scholar 

  • Sawada, N.: Electron microscope studies on sperm differentiation in marine annelid worms. II. Sperm formation in Arenicola brasiliensis. Develop. Growth Differ. 17, 89–99 (1975)

    Google Scholar 

  • Sawada, N.: Electron microscopical studies of spermatogenesis in polychaetes. Fortschr. Zool. 29, 99–114 (1984)

    Google Scholar 

  • Sawada, N., O. Osamu and M. Kubo: Electron microscope studies on sperm differentiation of marine annelid worms. I. Sperm formation in Ikedosoma gogoshimense. Dev. Growth Differ. 17, 77–87 (1975)

    Google Scholar 

  • Schroeder, P. C. and C. O. Hermans: Annelida: Polychaeta. In: Reproduction of marine invertebrates, vol. III, 343 pp. Ed. by A. C. Giese and J. S. Pearse. New York: Academic Press 1975

    Google Scholar 

  • Thiéry, J. P.: Mise en evidence des polysacharides sur coupes fines en microscopie électronique. J. Microsc. 6, 987–993 (1967)

    Google Scholar 

  • Webster, P. M. and K. S. Richards: Spermiogenesis in the enchytraeid Lumbricillus rivalis (Oligochaeta: Annelida). J. ultrastruc. Res. 61 62–77 (1977)

    Google Scholar 

  • Westheide, W.: Genesis and structure of the modified spermatozoon in the interstitial polychaete Hesionides arenaria. Biol. Cell. 50, 53–66 (1984)

    Google Scholar 

  • Wilson, D. P.: The larval stages of Notomastus latericeus Sars. J. mar. biol. Ass. U.K. 18, 511–518 (1933)

    Google Scholar 

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Authors and Affiliations

  1. Reproductive Biology Program, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, 33450, Fort Pierce, Florida, USA

    K. J. Eckelbarger

  2. Marine Biological Laboratory, 02543, Woods Hole, Massachusetts, USA

    J. P. Grassle

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  1. K. J. Eckelbarger
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  2. J. P. Grassle
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Communicated by J. M. Lawrence, Tampa

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Eckelbarger, K.J., Grassle, J.P. Spermatogenesis, sperm storage and comparative sperm morphology in nine species of Capitella, Capitomastus and Capitellides (Polychaeta: Capitellidae). Mar. Biol. 95, 415–429 (1987). https://doi.org/10.1007/BF00409572

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