The Korean Journal of Malacology (한국패류학회지)

The Malacological Society of Korea (한국패류학회)
권호 표지
DOI QR코드

DOI QR Code

Sex and Sex Reversal of Bivalves

이매패류의 성과 성전환

  • Lee, Jung Sick (Department of Aqualife Medicine, Chonnam National University)
  • 이정식 (전남대학교 수산생명의학과)
  • Received : 2015.11.20
  • Accepted : 2015.12.30
  • Published : 2015.12.30
Download PDF
⟨ Previous Next ⟩

Abstract

The sex of bivalves is classified into gonochorism and hermaphroditism, and hermaphroditism is further divided into simultaneous (synchronous or functional), and sequential (asynchronous). The sequential hermaphroditism signifies sex reversal in accordance with seasons. In general, in the case of gonochoristic bivalves, manifestation of sex as female and male, after having identified the morphological sex, is limited to a period of the life cycle in any given individual. In order to accurately identify sex, continuous monitoring of changes in the sex during life cycle is necessary by tagging the sex. In the bivalves, sex reversal and sequential hermaphroditism has been reported in the Ostreidae, Pectinidae, Veneridae and Arcidae etc.. Most of these studies have reached this conclusion based on evidence derived from sex ratio change in accordance with the age within same populations. Sex change in the sequential hermaphroditic bivalves normally occurs when the gonad is undifferentiated between spawning seasons. Two factors are involved in sex determination and sex change in bivalves, namely genetic and environmental. However, more detailed research is needed on the effect of the genetic and environmental factors involved in sex determination and sex change of bivalves.

이매패류의 성은 자웅이체와 자웅동체로 구분되며, 자웅이체는 동시자웅동체와 비동시자웅동체로 나누어진다. 비동시자웅동체는 계절에 따른 성의 전환을 의미한다. 일반적으로 자웅이체 이매패류의 경우 형태학적 성으로 표현되는 암, 수는 개체의 생활사 가운데 일정한 한 시기에 국한된 것이다. 개체의 성을 정확히 확인하기 위해서는 성을 표지한 후, 생활사 동안 성의 변화를 연속적으로 추적해야 한다. 이매패류에서 성전환과 비동시자웅동체는 굴과, 가리비과, 백합과 및 돌조개과 등의 이매패류에서 보고되고 있다. 이들 연구의 대부분은 동일 개체군에서 연령에 따른 성비의 변화를 증거로 이러한 결론에 도달하게 되었다. 비동시자웅동체 이매패류에서 성의 변화는 보통 방란, 방정 후 생식소의 비활성기에 일어난다. 이매패류에서 성결정과 성의 변화에는 유전적 요인과 환경적 요인 두 가지가 관여하지만, 이에 관한 이들의 영향에 관해서는 세부적인 연구가 필요하다.

Keywords

References

  1. Ackermann, G.E., Schwaiger, J., Negele, R.D. and Fent, K. (2002) Effects of long-term nonylphenol exposure on gonadal development and biomarkers of estrogenicity on juvenile rainbow trout, Oncorhynchus mykiss. Aquatic Toxicology, 60: 203-221. https://doi.org/10.1016/S0166-445X(02)00003-6
  2. Amemiya, I. (1925) Hermaphroditism in the Portuguese oyster. Nature, 116: 608.
  3. Amemiya, I. (1929) On the sex change of the Japanese common oyster, Ostrea gigas Thunberg. Proceeding of the Imperial Academy, 5: 284-286.
  4. Asif, M. (1979) Hermaphroditism and sex reversal in the four common oviparous species of oysters from the coast of Karachi. Hydrobiologia, 66: 49-55. https://doi.org/10.1007/BF00019139
  5. Barnes, R.D. (1987) The Mollusks. In; Invertebrate Zoology 5th. pp. 342-471, Saunders College Publishing, New York.
  6. Behzadi, S., Parivar, K. and Roustaian, P. (1997) Gonadal cycle of pearl oyster, Pinctada fucata (Gould) in northeast Persian Gulf, Iran. Journal of Shellfish Research, 16: 129-135.
  7. Britton, A.C. and Morton, B. (1982) A dissection guide, field and laboratory manual for the introduced bivalve Corbicula fluminea. Malacological Review, 3: 1-82.
  8. Burton, S.A., Johnson, G.R. and Davidson, T.J. (1996) Cytologic sexing of marine mussels (Mytilus edulis). Journal of Shellfish Research, 15: 345-347.
  9. Chang, Y.J. and Lee, T.Y. (1982) Gametogenesis and reproductive cycle of the cockle, Fulvia mutica (Reeve). Bulletin of the Korean Fisheries Society, 15: 241-253.
  10. Chavez-Villalba, J., Soyez, C., Huvet, A., Gueguen, Y., Lo, C. and Le Moullac, G. (2011) Determination of gender in the pearl oyster Pinctada margaritifera. Journal of Shellfish Research, 30: 231-240. https://doi.org/10.2983/035.030.0206
  11. Chung, E.Y., Ryou. D.K. and Lee, J.H. (1994) Gonadal development, age and growth of the shortnecked clam, Ruditapes philippinarum (Pelecypoda: Veneridae), on the coast of Kimje, Korea. The Korean Journal of Malacology, 10: 38-54.
  12. Coe, W.R. and Fox, D.L. (1942) Biology of the California sea-mussel (Mytilus californianus). I. Influence of temperature, food supply, sex and age in the rate of growth. Journal of Experimental Zoology, 90: 1-30. https://doi.org/10.1002/jez.1400900102
  13. Coe, W.R. (1934) Alternation of sexuality in oysters. American Naturalist, 68: 236-251. https://doi.org/10.1086/280542
  14. Coe, W.R. (1936a) Environment and sex in the oviparous oyster, Ostrea virginica. Biological Bulletin, 71: 353-359. https://doi.org/10.2307/1537440
  15. Coe, W.R. (1936b) Sex ratios and sex changes in mollusks. Memoires du Musee royal d'histoire naturelle de Belgique, 3: 69-76.
  16. Coe, W.R. (1938) Conditions influencing change of sex in mollusks of the genus Crepidula. Journal of Experimental Zoology, 77: 401-424. https://doi.org/10.1002/jez.1400770305
  17. Coe, W.R. (1943) Sexual differentiation in mollusks. I. Pelecypods. The Quarterly Review of Biology, 18: 154-164. https://doi.org/10.1086/394673
  18. Cole, H.A. (1942) Primary sex-phases in Ostrea edulis. Quarterly Journal of Microscopical Science, 83: 317-356.
  19. Collin, R. (2013) Phylogenetic patterns and phenotypic plasticity of molluscan sexual systems. Integrative and Comparative Biology, 53: 723-735. https://doi.org/10.1093/icb/ict076
  20. Conklin, E.G. (1897) The embryology of Crepidula, A contribution to the cell lineage and early development of some marine gastropods. Journal of Morphology, 13: 1-226. https://doi.org/10.1002/jmor.1050130102
  21. Conklin, E.G. (1898). Environmental and sexual dimorphism in Crepidula. Proceeding of the Academy of Natural Sciences Philadelphia, 50: 435-444.
  22. Eversole, A.G. (2001) Reproduction in Mercenaria mercenaria. In; Biology of the Hard Clam. (ed. by Kraeuter, J.N. and Castagna, M.). pp. 221-260,
  23. Elsevier, New York. Franz, D.R. (1973) The ecology and reproduction of a marine bivalve, Mysella planulata (Erycinacea). The Biological Bulletin, 144: 93-106. https://doi.org/10.2307/1540149
  24. Fretter, V. and Graham, A. (1964) Reproduction. In; Physiology of Mollusca. (ed. by Wilbur, K.M. and Yonge, C.M.). pp. 127-164, Academic Press, New York.
  25. Gagne, F., Blaise, C., Pellerin, J., Pelletier, E., Douville, M., Gauthier-Clerc, S. and Viglino, L. (2003) Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comparative Biochemistry and Physiology C, 134: 189-198. https://doi.org/10.1016/S1096-4959(02)00250-6
  26. Galtsoff, P.S. (1964) The American oyster Crassostrea virginica Gmelin. Fishery Bulletin, 64: 1-480.
  27. Garcia-Dominguez, F., Garcia-Gasca, S.A. and Castro-Ortiz, J.L. (1994) Spawning cycle of the red clam, Megapitaria aurantiaca (Sowerby, 1831) (Veneridae) at Isla Espiritu Santo, Baja California Sur, Mexico. Journal of Shellfish Research, 13: 417-423.
  28. Gosling, E. (2004) Bivalve Molluscs: Biology, Ecology and Culture. pp. 1-443, Blackwell Science, Oxford.
  29. Gould, H.N. (1952) Studies on sex in the hermaphrodite mollusk Crepidula plana. IV. Internal and external factors influencing growth and sex development. Journal of Experimental Zoology, 119: 93-163. https://doi.org/10.1002/jez.1401190107
  30. Guo, X., Hedgecock, D., Hershberger, W.K., Cooper, K. and Allen Jr., S.K. (1998) Genetic determinants of protandric sex in the Pacific oyster, Crassostrea gigas Thunberg. Evolution, 52: 394-402. https://doi.org/10.2307/2411076
  31. Heard, W.H. (1970) Hermaphroditism in Margarifera falcata (Gould) (Pelecypoda: Margaritiferidae). Nautilus, 83: 113-114.
  32. Heard, W.H. (1975) Sexuality and other aspects of reproduction in Anodonta (Pelecypoda: Unionidae). Malacologia, 15: 81-103.
  33. Heard, W.H. (1979) Hermaphroditism in Elliptio (Pelecypoda: Unionidae). Malacological Review, 12: 21-28.
  34. Heller, J. (1993) Hermaphroditism in molluscs. Biological Journal of the Linnean Society, 48: 19-42. https://doi.org/10.1111/j.1095-8312.1993.tb00874.x
  35. Jabbar, A. and Davies, J.I. (1987) A simple and convenient biochemical method for sex identification in the marine mussel, Mytilus edulis L.. Journal of Experimental Marine Biology and Ecology, 107: 39-44. https://doi.org/10.1016/0022-0981(87)90121-3
  36. Jeon, M.A., Park, M.W., Ku, K., Ju, S.M., Ko, P., Kim, B.H., Myeong, J.I. and Lee, J.S. (2012). Gonadal development and reproductive cycle of the boring bivalve, Barnea davidi (Deshayes, 1874) in Hampyeong Bay, Korea (Bivalvia: Pholadidae). Journal of Shellfish Research, 31: 951-958. https://doi.org/10.2983/035.031.0407
  37. Ju, S.M., Park, J.J. and Lee, J.S. (2009) Induction of intersex and masculinization of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae) by zinc. Animal Cells and Systems, 13: 339-344. https://doi.org/10.1080/19768354.2009.9647227
  38. Kim, D.H., Lee, W.O. and Lee, J.S. (2014) Reproductive ecology of the freshwater marsh clam, Corbicula papyracea (Heude) in Bukhan River. The Korean Journal of Malacology, 30: 107-116. https://doi.org/10.9710/kjm.2014.30.2.107
  39. Lee, J.H. (1997) Studies on the gonadal development and gametogenesis of the granulated ark, Tegillarca granosa (Linne). The Korean Journal of Malacology, 13: 55-64.
  40. Lee, J.S., Cho, H.S., Jin, Y.G., Park, J.J. and Shin, Y.K. (2009) Reproductive disrupting effect of organotin compound in the ark shell, Scapharca broughtonii (Bivalvia: Arcidae). Animal Cells and Systems, 13: 223-227. https://doi.org/10.1080/19768354.2009.9647214
  41. Lee, J.S., Ju, S.M., Park, J.S., Jin, Y.G., Shin, Y.K. and Park, J.J. (2010) Germ cell aspiration (GCA) method as a non-fatal technique for sex identification in two bivalves (Gomphina veneriformis and Tegillaca granosa). Development and Reproduction, 14: 7-11.
  42. Lee, J.S., Ku, K., Jeon, M.A., Kim, H., Kim, S., Choi, J.S., Park, J.J. and Shin, Y.K. (2014a) Sex ratio change of Tegillarca granosa (Bivalvia: Arcidae) with environmental factors. In; Proc. Aquaculture Europe 14, pp. 704-70, .Donostia-San Sebastian, Spain, 15-17 Oct. 2014.
  43. Lee, J.S., Ku, K., Kim, H., Park, J.S., Park, J.J., Shin, Y.K. and Jeon, M.A. (2012) Indirect evidence on sex reversal with sex ratio in Tegillarca granosa (Bivalvia: Arcidae) and Ruditapes philippinarum (Bivalvia: Veneridae). Development and Reproduction, 16: 177-183.
  44. Lee, J.S., Park, J.J., Shin, Y.K., Kim, H. and Jeon, M.A. (2014b) Sex change and sequential hermaphroditism of Tegillarca granosa (Bivalvia: Arcidae). Invertebrate Reproduction and Development, 58: 314-318. https://doi.org/10.1080/07924259.2014.949014
  45. Lee, J.S. and Park, J.J. (2007) Risk assessment of nonylphenol using the sex ratio, sexual maturation, intersex and lipofuscin accumulation of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae). Korean Journal of Fisheries and Aquatic Sciences, 40: 16-23. https://doi.org/10.5657/kfas.2007.40.1.016
  46. Lee, J.S., Park, J.S., Shin, Y.K., Lee, Y.G. and Park, J.J. (2013) Sequential hermaphroditism in Manila clam Ruditapes philippinarum (Bivalvia: Veneridae). Invertebrate Reproduction and Development, 57: 185-188. https://doi.org/10.1080/07924259.2012.717109
  47. Leonard, J.L. (2013) Williams' paradox and the role of phenotypic plasticity in sexual systems. Integrative and Comparative Biology, 53: 671-688. https://doi.org/10.1093/icb/ict088
  48. Mackie, G.L. (1984) Bivalves. In; The Mollusca, Vol. 7. Reproduction. (ed. by Tompa, A., Verdonk, N.H. and Biggelaar, J.A.). pp. 351-418, Academic Press, New York.
  49. Matozzo, V. and Marin, M.G. (2005) Can 4-nonylphenol induce vitellogenin-like proteins in the clam Tapes philippinarum? Environmental Research, 97: 43-49. https://doi.org/10.1016/j.envres.2004.03.002
  50. Menzel, W. (1989) The biology, fishery and culture of quahog clam, Mercenaria. In; Clam Culture in North America. (ed. by Manzi, J.J. and Castagna, M.). pp. 201-242, Elsevier Science Publishers B.V., Amsterdam.
  51. Mikailov, A.T., Torrado, M. and Mendez, J. (1995) Sexual differentiation of reproductive tissue in bivalve molluscs: identification of male associated polypeptide in the mantle of Mytilus galloprovincialis Lmk. Intenational Journal of Developmental Biology, 39: 545-548.
  52. Morcillo, Y. and Porte, C. (2000) Evidence of endocrine disruption in clams Ruditapes decussata transplanted to a tributyltin-polluted environment. Environmental Pollution, 107: 47-52. https://doi.org/10.1016/S0269-7491(99)00133-5
  53. Morton, B. (1991) Do the Bivalvia demonstrate environment-specific sexual strategies? A Hong-Kong model. Journal of Zoology, 223: 131-142. https://doi.org/10.1111/j.1469-7998.1991.tb04754.x
  54. Orton, J.H. (1909) On the occurrence of protandric hermaphroditism in the mollusc Crepidula fornicata. Proceeding of the Royal Society of London, 81B: 468-484.
  55. Orton, J.H. (1927) Observations and experiments on sex-change in the European oyster (O. edulis). Part I. The change from female to male. Journal of the Marine Biological Association of the United Kingdom, 14: 967-1045. https://doi.org/10.1017/S0025315400051183
  56. Orton, J.H. (1933) Observations and experiments on sex-change in the European oyster (O. edulis). Part III. On the fate of unspawned ova. Part IV. On the change from male to female. Journal of the Marine Biological Association of the United Kingdom, 19: 1-54. https://doi.org/10.1017/S0025315400055752
  57. Osanai, K. (1975) Seasonal gonad development and sex alteration in the scallop Patinopecten yessoensis. Bulletin of the Marine Biological Station of Asamushi Tokyo University, 15: 81-88.
  58. Park, J.J., Kim, H., Kang, S.W., An, C.M., Lee, S.H., Gye, M.C. and Lee, J.S. (2012) Sex ratio and sex reversal in two-year-old class of oyster, Crassostrea gigas (Bivalvia: Ostreidae). Development and Reproduction, 16: 385-388. https://doi.org/10.12717/DR.2012.16.4.385
  59. Park, J.J., Lee, J.Y., Lee, J.S. and Chang, Y.J. (2003) Gonadal development and gametogenic cycle of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae). Korean Journal of Fisheries and Aquatic Sciences, 36: 352-357. https://doi.org/10.5657/kfas.2003.36.4.352
  60. Park, J.J., Shin, Y.K., Hung, S.S.O., Romano, N., Cheon, Y.P. and Kim, J.W. (2015) Reproductive impairment and intersexuality in Gomphina veneriformis (Bivalvia: Veneridae) by the tributyltin compound. Animal Cells and Systems, 19: 61-68. https://doi.org/10.1080/19768354.2014.995225
  61. Park, J.S. and Lee, J.S. (2011) Change of reproductive and histological biomarkers of Ruditapes philippinarum (Bivalvia: Veneridae) exposed to nonylphenol. The Korean Journal of Malacology, 27: 181-190. https://doi.org/10.9710/kjm.2011.27.3.181
  62. Purchon, R.D. (1968) The Biology of the Mollusca. pp. 560, Pergamon, London.
  63. Rosewater, J. (1965) The family Tridacnidae in the Indo-Pacific. Indo-Pacific Mollusca, 1: 347-365.
  64. Sastry, A.N. (1979) Pelecypoda (excluding Ostreidae). In; Reproduction of Marine Invertebrates, Vol. 5. (ed. by Giese, A.C. and Pearse, P.J.). pp. 113-292, Academic Press, New York.
  65. Shin, Y.K., Park, J.J., Choi, J.S. and Lee, J.S. (2014) Indirect evidence on sex reversal of Sinonovacula comstricta (Bivalvia: Euheterodonta) and Gomphina veneriformis (Bivalvia: Veneridae). Development and Reproduction, 18: 73-78. https://doi.org/10.12717/DR.2014.18.2.073
  66. Thompson, R.J., Newell, R.I.E., Kennedy, V.S. and Mann, R. (1996) Reproductive process and early development. In; The Eastern Oyster Crassostrea virginica. (ed. by Kennedy, V.S., Newell, R.I.E. and Eble, A.F.) pp. 335-370, Maryland Sea Grant, College Park, Maryland.
  67. Tolls, J., Kloepper-Sams, P. and Sijm, D.T.H.M. (1994) Surfactant bioconcentration - A critical review. Chemosphere, 29: 693-719. https://doi.org/10.1016/0045-6535(94)90040-X
  68. Turner, R.D. (1966) A Survey and Illustrated Catalogue of the Teredinidae (Mollusca: Bivalvia). pp. 265, Harvard University Press, Cambridge.
  69. van der Schalie, H. and Locke, F. (1941) Hermaphroditism in Anodonta grandis a freshwater mussels. Science, 432: 1-7.
  70. van der Schalie, H. (1970) Hermaphroditism among North America freshwater mussels. Malacologia, 10: 93-112.
  71. Ventilla, R.F. (1982) The scallop industry in Japan. Advances in Marine Biology, 20: 310-382.
  72. Villalejo-Fuerte, M. and García-Dominguez, F. (1998) Reproductive cycle of Spondylus leucacanthus (Broderip, 1833) (Bivalvia: Spondylidae) at Isla Danzante, Gulf California. Journal of Shellfish Research, 17: 1037-1042.
  73. Walne, P.R. (1974) Culture of Bivalve Molluscs: 50 years' experience at Conwy. pp. 173, Fishing News (Books) Ltd., Surrey, England.
  74. Wi, C.H., Chang, Y.J., Lee, S.J., Hur, Y.B. and Lee, J.S. (2003) Sexual maturation and gametogenic cycle of the hard shelled mussel, Mytilus coruscus (Bivalvia: Mytilidae). Journal of Aquaculture, 16: 245-251.
  75. Wright, W.G. and Lindberg, D.R. (1979) A non-fetal method of sex determination for patellacean gastropods. Journal of the Marine Biological Association of the United Kingdom, 59: 803. https://doi.org/10.1017/S0025315400045793
  76. Wright, W.G. (1988) Sex change in the Mollusca. Trends in Ecology and Evolution, 3: 137-140. https://doi.org/10.1016/0169-5347(88)90177-2
  77. Yusa, Y. (2007) Causes of variation in sex ratio and modes of sex determination in the Mollusca-an overview. American Malacological Bulletin, 23: 89-98. https://doi.org/10.4003/0740-2783-23.1.89

Cited by

  1. Implications for Fisheries Management: Sex Ratio, Size at Sexual Maturity, and Reproductive Cycle of Saxidomus purpuratus (Bivalvia: Veneridae) in Korea vol.37, pp.5, 2015, https://doi.org/10.2983/035.037.0505