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Fine Structure of the Gametes in Rhynchospio glandulosa (Annelida: Spionidae), a Hermaphrodite Brooding Larvae on the Parent’s Dorsum

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Abstract

Rhynchospio glandulosa is a common polychaete living in silty tubes in soft sediments in temperate shallow waters in the Northwest Pacific. Worms are simultaneous hermaphrodites. Spermatogenesis occurs in the coelomic cavity. Spermatids are joined in 16-cell clusters. The spermatozoa have a dome-shaped acrosome 1.2 µm long, an elongated nucleus 2.9 µm long, midpiece 2.4 µm long with subspherical mitochondria, and a flagellum about 44 µm long. The acrosome is a complex structure with five internal parts. The nucleus is concave anteriorly and has a short fossa posteriorly which accommodates the basal body of the axoneme. The flagellum is strengthened by two circles of microtubules in addition to the central axoneme. Oogenesis is intraovarian. Developed oocytes are about 130 µm in diameter, with an envelope about 0.8 µm thick, consisting of three layers of extracellular matrix: the thickest basal layer penetrated by unbranched microvilli each about 0.4 µm long, a homogenous intermediate layer with the highest electron density, and the outer brush-like layer with numerous extensions each about 0.3 µm long. The oocytes are spawned to the parent’s dorsum where they are loosely held by flat branchiae and long dorsal capillaries. In this “hatchery” larvae develop until the four-segment stage, then leave the parent and continue development in sea water. The general morphology of long-headed spermatozoa and thin-envelope oocytes of R. glandulosa is similar to that of other brooding spionids, but the details of their gamete ultrastructure are different.

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REFERENCES

  1. Lee, G.H. and Min, G.-S., Rhynchospio aciliata sp. nov., a new spionid species (Annelida, Spionidae) from the Korea Strait, ZooKeys, 2022, vol. 1100, pp. 191–205. https://doi.org/10.3897/zookeys.1100.80077

    Article  PubMed  PubMed Central  Google Scholar 

  2. Radashevsky, V.I., Malyar, V.V., Pankova, V.V., et al., Molecular analysis of six Rhynchospio Hartman, 1936 species (Annelida: Spionidae) with comments on the evolution of brooding within the group, Zootaxa, 2016, vol. 4127, pp. 579–590. https://doi.org/10.11646/zootaxa.4127.3.10

    Article  PubMed  Google Scholar 

  3. Radashevsky, V.I., Morphology and biology of a new Rhynchospio species (Polychaeta: Spionidae) from the South China Sea, Vietnam, with the review of Rhynchospio taxa, J. Nat. Hist., 2007, vol. 41, pp. 985–997. https://doi.org/10.1080/00222930701376717

    Article  Google Scholar 

  4. Radashevsky, V.I. and Choi, J.-W., Morphology and reproductive biology of a new hermaphroditic Rhynchospio (Annelida: Spionidae) species brooding larvae on the parent’s dorsum, Mar. Biodiversity, 2021, vol. 51, pp. 1–15. https://doi.org/10.1007/s12526-021-01197-6

    Article  Google Scholar 

  5. Hannerz, L., Larval development of the polychaete families Spionidae Sars, Disomidae Mesnil, and Poecilochaetidae n. fam. in the Gullmar Fjord (Sweden), Zool. Bidr. Uppsala, 1956, vol. 31, pp. 1–204.

    Google Scholar 

  6. Söderström, A., Studien über die Polychätenfamilie Spionidae. Inaugural-Dissertation, Uppsala: Almquist & Wicksells, 1920.

    Google Scholar 

  7. Blake, J.A., Spionida, in Reproductive Biology and Phylogeny of Annelida, Reproductive Biology and Phylogeny, vol. 4, Enfield: Science, 2006, pp. 565–638.

  8. Blake, J.A. and Arnofsky, P.L., Reproduction and larval development of the spioniform Polychaeta with application to systematics and phylogeny, Hydrobiologia, 1999, vol. 402, pp. 57–106. https://doi.org/10.1023/A:1003784324125

    Article  Google Scholar 

  9. Eckelbarger, K.J., An ultrastructural study of oogenesis in Streblospio benedicti (Spionidae), with remarks on diversity of vitellogenic mechanisms in Polychaeta, Zoomorphology, 1980, vol. 94, pp. 241–263.

    Article  Google Scholar 

  10. Fonsêca-Genevois, V. and Cazaux, C., Streblospio benedicti Webster, 1879 (Annélide Polychète) dans l’estuaire de la Loire: biologie et écologie, Cah. Biol. Mar., 1987, vol. 28, pp. 231–261.

    Google Scholar 

  11. Levin, L.A., Multiple patterns of development in Streblospio benedicti Webster (Spionidae) from three coasts of North America, Biol. Bull., 1984, vol. 166, pp. 494–508.

    Article  Google Scholar 

  12. Dean, D., On the reproduction and larval development of Streblospio benedicti Webster, Biol. Bull., 1965, vol. 128, pp. 67–76.

    Article  Google Scholar 

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

    Article  Google Scholar 

  14. Franzén, Å., On spermiogenesis, morphology of the spermatozoon, and biology of fertilization among invertebrates, Zool. Bidr. Uppsala, 1956, vol. 31, pp. 355–482.

    Google Scholar 

  15. Jamieson, B.G.M. and Rouse, G.W., The spermatozoa of the Polychaeta (Annelida): An ultrastructural review, Biol. Rev., 1989, vol. 64, pp. 93–157.

    Article  CAS  PubMed  Google Scholar 

  16. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 2012, vol. 9, pp. 671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Sato, M. and Osanai, K., Sperm reception by an egg microvillus in the polychaete, Tylorrhynchus heterochaetus, J. Exp. Zool., 1983, vol. 227, pp. 459–469. https://doi.org/10.1002/jez.1402270315

    Article  Google Scholar 

  18. Sato, M. and Osanai, K., Morphological identification of sperm receptors above egg microvilli in the polychaete, Neanthes japonica, Dev. Biol., 1986, vol. 113, pp. 263–270. https://doi.org/10.1016/0012-1606(86)90161-2

    Article  CAS  PubMed  Google Scholar 

  19. Fitzpatrick, J.L., Kahrl, A.F., and Snook, R.R., SpermTree, a species-level database of sperm morphology spanning the animal tree of life, Sci. Data, 2022, vol. 9, pp. 1–6. https://doi.org/10.1038/s41597-022-01131-w

    Article  Google Scholar 

  20. Purschke, G. and Fursman, M.C., Spermatogenesis and spermatozoa in Stygocapitella subterranea (Annelida, Parergodrilidae), an enigmatic supralittoral polychaete, Zoomorphology, 2005, vol. 124, pp. 137–148.

    Article  Google Scholar 

  21. Purschke, G. and Jördens, J., Male genital organs in the eulittoral meiofaunal polychaete Stygocapitella subterranea (Annelida, Parergodrilidae): Ultrastructure, functional and phylogenetic significance, Zoomorphology, 2007, vol. 126, pp. 283–297. https://doi.org/10.1007/s00435-007-0047-z

    Article  Google Scholar 

  22. Westheide, W., The concept of reproduction in polychaetes with small body size: Adaptations in interstitial species, in Polychaete Reproduction: Progress in Comparative Reproductive Biology, Fortschritte der Zoologie, vol. 29, Stuttgart: Gustav Fischer, 1984, pp. 265–287.

    Google Scholar 

  23. Olive, P.J.W., Annelida-Polychaeta, in Reproductive Biology of Invertebrates, vol. 2: Spermatogenesis and Sperm Function, New York: Wiley, 1983, pp. 321–342.

  24. Bochert, R., An electron microscopic study of oogenesis in Marenzelleria viridis (Verrill 1873) (Polychaeta; Spionidae) with special reference to large cortical alveoli, Invertebr. Reprod. Dev., 1996, vol. 29, pp. 57–69. https://doi.org/10.1080/07924259.1996.9672495

    Article  Google Scholar 

  25. Radashevsky, V.I., Yurchenko, O.V., and Alexandrova, Y.N., Fine structure of the gametes and spermiogenesis in Spiophanes uschakowi (Annelida: Spionidae) from the Sea of Japan, with comments on fertilization biology in broadcast-spawning spionids, Micron, 2018, vol. 115, pp. 32–40. https://doi.org/10.1016/j.micron.2018.08.005

    Article  PubMed  Google Scholar 

  26. Eckelbarger, K.J., Polychaeta: Oogenesis, in Microscopic Anatomy of Invertebrates, vol. 7: Annelida, New York: Wiley-Liss, 1992, pp. 109–127.

  27. Eckelbarger, K.J., Comparative aspects of oogenesis in polychaetes, in Polychaete Reproduction: Progress in Comparative Reproductive Biology, Fortschritte der Zoologie, vol. 29, Stuttgart: Gustav Fisher, 1984, pp. 123–148.

    Google Scholar 

  28. Eckelbarger, K.J., Oogenesis and oocytes, Hydrobiologia, 2005, vol. 535–536, pp. 179–198.

    Google Scholar 

  29. Rice, S.A. and Reish, D.J., Egg capsule formation in the polychaete Polydora ligni: Confirmation of a hypothesis, Bull. South. Calif. Acad. Sci., 1976, vol. 75, pp. 285–286.

    Google Scholar 

  30. Blake, J.A., Reproduction and larval development of Polydora from northern New England (Polychaeta: Spionidae), Ophelia, 1969, vol. 7, pp. 1–63.

    Article  Google Scholar 

  31. Campbell, M.A., Larval development of Streblospio benedicti Webster, Biol. Bull., 1957, vol. 113, pp. 336–337.

    Google Scholar 

  32. Tyler, A., The biology and chemistry of fertilization, Am. Nat., 1965, vol. 99, pp. 309–334. https://doi.org/10.1086/282374

    Article  Google Scholar 

  33. Cross, N.L., Fertilization in Urechis caupo and in polychaetes, in Polychaete Reproduction: Progress in Comparative Reproductive Biology, Fortschritte der Zoologie, vol. 29, Stuttgart: Gustav Fisher, 1984, pp. 149–166.

    Google Scholar 

  34. Franzén, Å. and Rice, S.A., Spermatogenesis, male gametes and gamete interactions, in The Ultrastructure of Polychaeta. Microfauna Marina 4, Stuttgart: Gustav Fischer, 1988, pp. 309–333.

    Google Scholar 

  35. Franklin, L.E., An egg cell-membrane derivative on the vitelline membrane of annelid eggs, Exp. Cell Res., 1966, vol. 43, pp. 673–675.

    Article  CAS  PubMed  Google Scholar 

  36. Gwynn, I. and Jones, P.C.T., On the egg investments and fertilization reaction in Pomatoceros triqueter L. An ultrastructural study, Z. Zellforsch. Mikrosk. Anat., 1971, vol. 113, pp. 388–396. https://doi.org/10.1007/BF00968546

    Article  CAS  PubMed  Google Scholar 

  37. Eckelbarger, K.J., Oogenesis and female gametes, in The Ultrastructure of Polychaeta. Microfauna Marina 4, Stuttgart: Gustav Fischer, 1988, pp. 281–307.

    Google Scholar 

  38. Giangrande, A., Licciano, M., Pagliara, P., et al., Gametogenesis and larval development in Sabella spallanzanii (Polychaeta: Sabellidae) from the Mediterranean Sea, Mar. Biol. (Berlin), 2000, vol. 136, pp. 847–861.

    Article  Google Scholar 

  39. Radashevsky, V.I., Alexandrova, Y.N., and Yurchenko, O.V., Spermiogenesis and spermatozoa ultrastructure of Aonides oxycephala (Annelida: Spionidae) from the Sea of Japan, Invertebr. Reprod. Dev., 2011, vol. 55, pp. 168–174. https://doi.org/10.1080/07924259.2011.553410

    Article  Google Scholar 

  40. Radashevsky, V.I., Reunov, A.A., Yurchenko, O.V., et al., Ultrastructure of spermatozoa of Prionospio japonica (Annelida: Spionidae) from Taiwan, Zool. Stud., 2010, vol. 49, pp. 265–269.

    Google Scholar 

  41. Bochert, R., An electron microscopic study of spermatogenesis in Marenzelleria viridis (Verrill, 1873) (Polychaeta; Spionidae), Acta Zool. (Stockholm), 1996, vol. 77, pp. 191–199.

    Article  Google Scholar 

  42. Rouse, G.W., An ultrastructural study of the spermatozoa from Prionospio cf. queenslandica and Tripolydora sp.: Two spionid polychaetes with different reproductive methods, Acta Zool. (Stockholm), 1988, vol. 69, pp. 205–216. https://doi.org/10.1111/j.1463-6395.1988.tb00917.x

    Article  Google Scholar 

  43. Radashevsky, V.I., Yurchenko, O.V., Tyurin, S.A., et al., Spermatogenesis and spermatozoa ultrastructure of two Dipolydora species (Annelida: Spionidae) from the Sea of Japan, Micron, 2015, vol. 69, pp. 43–55. https://doi.org/10.1016/j.micron.2014.11.004

    Article  PubMed  Google Scholar 

  44. Gao, Y., Zhang, T., Zhang, L., et al., Ultrastructure developments during spermiogenesis in Polydora ciliata (Annelida: Spionidae), a parasite of mollusca, J. Ocean Univ. China, 2014, vol. 13, pp. 1071–1077. https://doi.org/10.1007/s11802-014-2309-y

    Article  CAS  Google Scholar 

  45. Eckelbarger, K.J. and Hodgson, A.N., Ultrastructure of spermiogenesis and synthesis of enigmatic cytoplasmic inclusions in the spirally shaped spermatozoon of the polychaete Spio setosa (Annelida: Spionidae), Invertebr. Biol., 2014, vol. 133, pp. 146–157. https://doi.org/10.1111/ivb.12049

    Article  Google Scholar 

  46. Reunov, A.A., Yurchenko, O.V., Alexandrova, Y.N., et al., Spermatogenesis in Boccardiella hamata (Polychaeta: Spionidae) from the Sea of Japan: Sperm formation mechanisms as characteristics for future taxonomic revision, Acta Zool. (Stockholm), 2010, vol. 91, pp. 447–456. https://doi.org/10.1111/j.1463-6395.2009.00435.x

    Article  Google Scholar 

  47. Rice, S.A. and Rice, K.A., Variable modes of larval development in the Polydora cornuta complex (Polychaeta: Spionidae) are directly related to stored sperm availability, Zoosymposia, 2009, vol. 2, pp. 397–414.

    Article  Google Scholar 

  48. Vortsepneva, E.V., Zhadan, A.E., and Tzetlin, A.B., Spermiogenesis and sperm ultrastructure of Asetocalamyzas laonicola Tzetlin, 1985 (Polychaeta), an ectoparasite of the large spionid Scolelepis cf. matsugae Sikorsfi, 1994, from the White Sea, Sci. Mar., 2006, vol. 70, pp. 343–350.

    Article  Google Scholar 

  49. Williams, J.D., Spermiogenesis and spermatozoon ultrastructure of Polydora neocaeca (Polychaeta: Spionidae) from Rhode Island, Invertebr. Reprod. Dev., 2000, vol. 38, pp. 123–129.

    Article  Google Scholar 

  50. Rice, S.A., Polychaeta: spermatogenesis and spermiogenesis, in Microscopic Anatomy of Invertebrates, vol. 7: Annelida, New York: Wiley-Liss, 1992, pp. 129–151.

  51. Franzén, Å., Sperm ultrastructure in some Polychaeta, in The Functional Anatomy of the Spermatozoon, Proceedings of the second international symposium, Wenner-Gren Center, Stockholm: Pergamon, 1974, pp. 267–278.

  52. Gibson, G., MacDonald, K., and Dufton, M., Morphogenesis and phenotypic divergence in two developmental morphs of Streblospio benedicti (Annelida, Spionidae), Invertebr. Biol., 2010, vol. 129, pp. 328–343. https://doi.org/10.1111/j.1744-7410.2010.00213.x

    Article  Google Scholar 

  53. Vortsepneva, E., Tzetlin, A., and Tsitrin, E., Anterior muscular system of the dwarf ectoparasitic male Scolelepis laonicola (Tzetlin, 1985) (Polychaeta, Spionidae), Zoosymposia, 2009, vol. 2, pp. 429–435.

    Article  Google Scholar 

  54. Vortsepneva, E., Tzetlin, A., and Tsitrin, E., Nervous system of the dwarf ectoparasitic male of Scolelepis laonicola (Polychaeta, Spionidae), Zoosymposia, 2009, vol. 2, pp. 437–445.

    Article  Google Scholar 

  55. Vortsepneva, E., Tzetlin, A., Purschke, G., et al., The parasitic polychaete known as Asetocalamyzas laonicola (Calamyzidae) is in fact the dwarf male of the spionid Scolelepis laonicola (comb. nov.), Invertebr. Biol., 2008, vol. 127, pp. 403–416. https://doi.org/10.1111/j.1744-7410.2008.00137.x

    Article  Google Scholar 

  56. Jamieson, B.G.M., A comparison of spermiogenesis and spermatozoal ultrastructure in megascolecid and lunibricid carthworms (Oligochaeta: Annelida), Aust. J. Zool., 1978, vol. 26, pp. 225–240.

    Article  Google Scholar 

  57. Baccetti, B. and Afzelius, B.A., The Biology of the Sperm Cell (Monographs in Developmental Biology), Basel: Karger, 1976, vol. 10.

    Google Scholar 

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ACKNOWLEDGMENTS

We express our sincere gratitude to Denis V. Fomin for technical support with electron microscopes, Vladimir V. Yushin for comments during the preparation of the manuscript, as well as two anonymous reviewers for their comments and important suggestions.

Funding

This study was supported by the Government of the Russian Federation (Federal scientific and technical Program in the field of environmental development of the Russian Federation and climate change for 2021–2030; project no. 123080800009-5).

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  1. Zhirmunsky National Scientific Center of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, Vladivostok, Russia

    V. I. Radashevsky & O. V. Yurchenko

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Paper published in connection with the 50th anniversary of the Laboratory of Embryology of Zhirmunsky National Research Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences.

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Radashevsky, V.I., Yurchenko, O.V. Fine Structure of the Gametes in Rhynchospio glandulosa (Annelida: Spionidae), a Hermaphrodite Brooding Larvae on the Parent’s Dorsum. Russ J Mar Biol 49 (Suppl 1), S47–S60 (2023). https://doi.org/10.1134/S1063074023080072

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