Genetic, abiotic and social influences on sex differentiation in cichlid fishes and the evolution of sequential hermaphroditism

Fish and Fisheries

Volumn 6, Issue 2, 2005, Pages 93-110

  Oldfield, Ronald George ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Cichlid; Environmental sex determination; Hermaphroditism; Sex change; Sexual lability

Indexed keywords

CICHLID; HERMAPHRODITISM; SEX DETERMINATION;

AMPHILOPHUS CITRINELLUS; ANTHOZOA; CICHLIDAE; CRENICARA PUNCTULATA; PISCES;

EID: 22044444702     PISSN: 14672960     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1467-2979.2005.00184.x     Document Type: Review

References (112)

1. Abucay, J.S., Mair, G.C., Skibinski, D.O.F. and Beardmore, J.A. (1999) Environmental sex determination; the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173, 219-234.
2. Alberch, P., Gould, S.J., Oster, G.F. and Wake, D.B. (1979) Size and shape in ontogeny and phylogeny. Paleobiology 5, 296-317.
3. Ali, M., Nicieza, A. and Wootton, R.J. (2003) Compensatory growth in fishes: a response to growth depensation. Fish and Fisheries 4, 147-190.
4. Allsop, D.J. and West, S.A. (2003) Changing sex at the same relative body size. Nature 425, 783-784.
5. Aronson, L.R. (1948) Problems in the behaviour and physiology of a species of an African mouthbreeding fish. Transactions of the New York Academy of Sciences 2, 33-42.
6. Aronson, L.R. (1951) Factors influencing the spawning frequency in the cichlid fish. Tilapia macrocephala. American Museum Noviates 1484, 1-26.
7. Atz, J.A. (1964) Intersexuality in fishes. In: Intersexuality (eds C.N. Armstrong and A.J. Marshall), Academic Press, London, pp. 145-232.
8. Baca Hovey, C., Allen, L.G. and Hovey, T.E. (2002) The reproductive pattern of barred sand bass (Paralabrax nebulifer) from southern California. California Cooperative Oceanic Fisheries Investigations, Reports 43, 174-181.
9. Baerends, G.P. and Baerends-van Roon, J.M. (1950) An introduction to the study of the ethology of cichlid fishes. Behaviour (Suppl. 1), 235 pp.
10. Baras, E., Prignon, C., Gohoungo, G. and Mélard, C. (2000) Phenotypic sex differentiation of blue tilapia under constant and fluctuating thermal regimes and its adaptive and evolutionary implications. Journal of Fish Biology 57, 210-223.
11. Barlow, G.W. (1970) A test of appeasement and arousal hypotheses of courtship behaviour in a cichlid fish, Etroplus maculatus. Zeitschrift für Tierpsychologie 27, 779-806.
12. Barlow, G.W. (1976) The Midas cichlid in Nicaragua. In: Investigations of the Ichthyofauna of Nicaraguan Lakes (ed. T.B. Thorson). School of Life Sciences, University of Nebraska, Lincoln, Nebraska, pp. 333-358.
13. Barlow, G.W. (1993) The puzzling paucity of feeding territories among freshwater fishes. Marine Behavior and Physiology 23, 155-174.
14. Barlow, G.W. (2000) The Cichlid Fishes, Nature's Grand Experiment in Evolution. Perseus Publishing, Cambridge, MA.
15. Barlow, G.W. (2001) Parsing mouth brooding in cichlid fishes to illuminate the course of evolution. Journal of Aquariculture and Aquatic Sciences, Cichlid Research: State of the Art 9, 66-78.
16. Baroiller, J., Chourrout, D., Fostier, A. and Jalabert, B. (1995) Temperature and sex chromosomes govern sex ratios of the mouthbrooding cichlid fish Oreochromis niloticus. Journal of Experimental Zoology 273, 216-223.
17. Baroiller, J.F., Nakayama, I., Foresti, F. and Chourrout, D. (1996) Sex determination studies in two species of teleost fish. Oreochromis niloticus and Leporinus elongatus. Zoological Studies 35, 279-285.
18. Brown, M.E. (1957) Experimental studies of growth. In: Physiology of Fishes, Vol. 1 (ed. M.E. Brown), Academic Press, New York, pp. 361-400.
19. Brown, J.L. (1964) The evolution of diversity in avian territorial systems. Wilson Bulletin 76, 160-169.
20. Bushman, P.J. and Burns, J.R. (1994) Social control of male maturation in the swordtail characin, Corynopoma riisei. Journal of Fish Biology 44, 263-272.
21. Buxton, C.D. and Garrett, P.A. (1990) Alternative reproductive styles in seabreams (Pisces: sparidae). Environmental Biology of Fishes 28, 113-124.
22. Carrasco, L.A.P., Penman, D.J. and Bromage, N. (1999) Evidence for the presence of sex chromosomes in Nile tilapia (Oreochromis niloticus) from synaptonemal complex analysis of XX, XY, and YY genotypes. Aquaculture 173, 207-218.
23. Carrillo, M., Zanuy, S., Blázquez, M., Ramos, J., Piferrer, F. and Donaldson, E.M. (1995) Sex control and ploidy manipulation in sea bass. In: Environmental Impacts of Aquatic Biotechnology. OECD documents, Paris, France, pp. 125-143.
24. Carruth, L.L. (2000) Freshwater cichlid Crenicara punctulata is a protogynous sequential hermaphrodite. Copeia 2000, 71-82.
25. Clemens, H.P. and Inslee, T. (1968) The production of unisexual broods by Tilapia mossambica sex reversed with methyltestosterone. Transactions of the American Fisheries Society 97, 18-21.
26. Conover, D.O. and Heins, S.W. (1987) Adaptive variation in environmental and genetic sex determination in a fish. Science 213, 577-579.
27. Davis, M.R. and Fernald, R.D. (1990) Social control of neuronal soma size. Journal of Neurobiology 21, 1180-1188.
28. Desprez, D. and Melard, C. (1998) Effect of ambient water temperature on sex determinism in the blue tilapia Oreochromis aureus. Aquaculture 162.,79-84.
29. Devlin, R.H. and Nagahama, Y. (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191-364.
30. Devlin, R.H., McNiel, B.K., Groves, T.D.D. and Donaldson, E.M. (1991) Isolation of a Y-chromosomal DNA probe capable of determining genetic sex in Chinook salmon (Oncorhynchus tshawytscha). Canadian Journal of Fisheries and Aquatic Sciences 48, 1606-1612.
31. Emlen, S.T. and Oring, L.W. (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197, 215-223.
32. Faunce, C.H., Patterson, H.M. and Lorenz, J.J. (2002) Age, growth, and mortality of the Mayan cichlid (Cichlasoma urophthalmus) from the southeastern Everglades. Fisheries Bulletin 100, 42-50.
33. Fernald, R.D. and Hirata, N.R. (1977) Field study of Haplochromis burtoni; quantitative behavioural observations. Animal Behaviour 32, 964-975.
34. Fink, W.L. (1982) The conceptual relationship between ontogeny and phylogeny. Paleobiology 8, 254-264.
35. Fishelson, L. (1970) Protogynous sex reversal in the fish Anthias squamipinnis (Teleostei: Anthiidae) regulated by the presence or absence of male fish. Nature 227, 90-91.
36. Fraley, N.B. and Fernald, R.D. (1982) Social control of developmental rate in the African cichlid, Haplochromis burtoni. Zeitschrift für Tierpsychologie 60, 66-82.
37. Francis, R.C. (1984) The effects of bidirectional selection for social dominance on agonistic behaviour and sex ratios in the Paradise fish (Macropodus opercularis). Behaviour 90, 25-45.
38. Francis, R.C. (1990) Temperament in a fish: a longitudinal study of the development of individual differences in aggression and social rank in the Midas cichlid. Ethology 86, 311-325.
39. Francis, R.C. (1992) Sexual lability in teleosts: developmental factors. The Quarterly Review of Biology 67, 1-18.
40. Francis, R.C. and Barlow, G.W. (1993) Social control of primary sex differentiation in the Midas cichlid. Proceedings of the National Academy of Science of the United States of America 90, 10673-10675.
41. Fricke, H.W. and Fricke, S. (1977) Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266, 830-832.
42. Fryer, G. and Iles, T.D. (1972) The Cichlid Fishes of the Great lakes of Africa: Their Biology and Evolution. Oliver and Boyd. Edinburgh, UK.
43. George, T. and Pandian, T.J. (1996) Hormonal induction of sex reversal and progeny testing in the zebra cichlid Cichlasoma nigrofasciatum. Journal of Experimental Zoology 275, 374-382.
44. Ghiselin, M.T. (1969) The evolution of hermaphroditism among animals. Quarterly Review of Biology 44, 189-208.
45. Godwin, J.R. (1994) Histological aspects of protandrous sex change in the anemonefish Amphiprion melanopus. Journal of Zoology (London) 232, 199-213.
46. Godwin, J., Crews, D. and Warner, R.R. (1996) Behavioural sex change in the absence of gonads in a coral reef fish. Proceedings of the Royal Society of London B 263, 1683-1688.
47. Goodwin, N.B., Balshine, S. and Reynolds, J.D. (1998) Evolutionary trends in parental care in cichlid fish. Proceedings of the Royal Society of London B 265, 2265-2272.
48. Gould, S.J. (1977) Ontogeny and Phylogeny. Harvard University Press, Cambridge, MA.
49. Grant, J.W.A. (1997) Territoriality. In: Behavioural Ecology of Teleost Fishes (ed. J.-G.J. Godin), Oxford University Press, Oxford, pp. 81-103.
50. Greenberg, B. (1961) Spawning and parental behaviour in female pairs of the jewelfish, Hemichromis bimaculatus, Gill. Behaviour 18, 44-61.
51. Griffiths, R., Orr, K.J., Adam, A. and Barber, I. (2000) DNA sex identification in the three-spined stickleback. Journal of Fish Biology 57, 1331-1334.
52. Guerrero, R.D. (1975) Use of androgens for the production of all-male Tilapia aurea (Steindachner). Transactions of the American Fisheries Society 104, 342-348.
53. Guerrero, R.D. and Shelton, W.L. (1974) An acetocarmine squash method for sexing juvenile fish. Progressive Fish Culturist 36, 56.
54. Hackmann, E. and Reinboth, R. (1974) Delimitation of the critical stage of hormone-influenced sex differentiation in Hemihaplochromis multicolor (Hilgendorf) (Cichlidae). General and Comparative Endocrinology 22, 42-53.
55. Harnish, C. (2004) Sex Allocation and Social Behaviour of Tramitichromis intermedius (Pisces: Cichlidae). Masters thesis. Boston University, Boston, MA. 54 pp.
56. Heiligenberg, W. (1965) Color polymorphism in the males of an African cichlid fish. Journal of Zoology (London) 146, 95-97.
57. Hickling, C.F. (1960) The Malacca Tilapia hybrids. Journal of Genetics 57, 1-10.
58. Hunter, G.A. and Donaldson, E.M. (1983) Hormonal sex control and its application to fish culture, In: Fish Physiology, Vol. 9B (eds W.S. Hoar, D.J. Randall and E.M. Donaldson). Academic Press, London, pp. 223-303.
59. Itzkowitz, M., Santangelo, N. and Richter, M. (2001) Parental division of labour and the shift from minimal to maximal role specializations: an examination using a biparental fish. Animal Behaviour 61, 1237-1245.
60. Jalabert, B., Moreau, J., Planquette, P. and Billard, R. (1974) Déterminismedu du sexe chez Tilapia macrochir et Tilapia nilotica: action de la méthyltestostérone dans l'alimentation des alevins sur la différenciation sexuelle; proportion des sexes dans la descendance des mâles inversés. Annales de Biologie Animale Biochimie et Biophysique 14, 729-739.
61. Kallman, K.D. (1984) A new look at sex determination in poeciliid fishes. In: Evolutionary Genetics of Fishes (ed. B.J. Turner). Plenum Press, New York, NY, pp. 95-172.
62. Kolluru, G.R. and Reznick, D.N. (1996) Genetic and social control of male maturation in Phallichthys quadripunctatus (Pisces: Poeciliidae). Journal of Evolutionary Biology 9, 695-715.
63. Kornfield, I. (1984) Descriptive genetics of cichlid fishes. In: Evolutionary Genetics of Fishes (ed. B.J. Turner). Plenum Press, New York, pp. 591-616.
64. Langston, R.C. (2004) Gonad Morphology and Sex Change in Sandburrowers (Teleostei: Creediidae). PhD Dissertation. University of Hawaii, Manoa, 138 pp.
65. Lee, B.Y., Penman, D.J. and Kocher, T.D. (2003) Identification of a sex-determining region in Nile tilapia (Oreochromis niloticus) using bulked segregant analysis. Animal Genetics 34, 1-5.
66. Liu, Z., Moore, P.H., Ma, H. et al. (2004) A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427, 348-352.
67. Loir, M., Canty, C. and LeBail, P.-Y. (1989) Ambisexuality in a South American cichlid: Satanoperca aff leucosticta. Aquatic Living Resources 2, 185-187.
68. Lowe-McConnell, R.H. (1975) Fish Communities in Tropical Fresh-waters: Their Distribution, Ecology, and Evolution. Longman, London, 337 pp.
69. Marchand, O., Govoroun, M., D'Cotta, H. et al. (2002) DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochimica et Biophysica Acta 1493, 180-187.
70. Matsuda, M., Nagahama, Y., Shinomiya, A. et al. (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417, 559-563.
71. McKaye, K.R. (1977) Defense of a predator's young by a herbivorous fish: an unusual strategy. American Naturalist 111, 301-315.
72. Meijide, F.J., Nostro, F.L.L. and Guerrero, G.A. (2005) Gonadal development and sex differentiation in the cichlid fish Cichlasome dimerus (Teleostei, perciformes): a light- and electron-microscopic study. Journal of Morphology 264, 191-210.
73. Naish, K.A. and Ribbink, A.J. (1990) A preliminary investigation of sex change in Pseudotropheus lombardoi (Pisces: Cichlidae). Environmental Biology of Fishes 28, 285-294.
74. Nakamura, M., Kobayashi, T., Chang, X.T. and Nagahama, Y. (1998) Gonadal sex differentiation in teleost fish. Journal of Experimental Zoology 281, 362-372.
75. Nakashima, Y., Sakai, Y., Karino, K. and Kuwamura, T. (2000) Female-female spawning and sex change in a haremic coral-reef fish, Labroides dimidiatus. Zoological Science 17, 967-970.
76. Nanda, I., Kondo, M., Hornung, U. et al. (2002) A duplicated copy of DMRT1 in the sex determining region of the Y chromosome of the medaka, Oryzias latipes. Proceedings of the National Academy of Science 99, 11778-11783.
77. Ohm, D. (1978) Sexualdimorphismus, Polygamie und Geschlechtswechsel bei Crenicara punctulata Gunther 1863 (Cichlidae, Teleostei). Sitzungs-berichte der Gesellschaft für Naturforschender Fruende zu Berlin 18, 90-104.
78. Ohm, D. (1980) Weibchen werden zu Maenchen: Geschlechtswechsel beim Buntbarsh Crenicara punctulata. Aqurien Magazin 14, 631-634.
79. Oliveira, R.F. and Canario, A.V.M. (2001) Hormones and social behaviour in cichlid fishes: a case study in the Mozambique tilapia. Journal of Aquariculture and Aquatic Sciences. Cichlid Research: State of the Art 9, 187-207.
80. Pandian, T.J. and Koteeswaran, R. (1999) Lability of sex differentiation in fish. Current Science 76, 580-583.
81. Peters, H.M. (1975) Hermaphroditism in cichlid fishes. In: Intersexuality in the Animal Kingdom (ed. R. Reinboth). Springer-Verlag, New York, pp. 228-235.
82. Polder, J.J.W. (1971) On gonads and reproductive behaviour in the cichlid fish Aequidens portalegrensis (Hensel). Netherlands Journal of Zoology 21, 265-365.
83. Reilly, S.M., Wiley, E.O. and Meinhardt, D.J. (1997) An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biological Journal of the Linnean Society 60, 119-143.
84. Robertson, D.R. and Warner, R.R. 1978. Sexual patterns in the Labroid fishes of the Western Caribbean. II: the parrotfishes (Scaridae). Smithsonian Contributions to Zoology 255, 1-26.
85. Robertson, D.R. (1972) Social control of sex reversal in a coral reef fish. Science 171, 1007-1009.
86. Römer, U. and Beisenherz, W. (1996) Environmental determination of sex in Apistogramma (Cichlidae) and two other freshwater fishes (Teleostei). Journal of Fish Biology 48, 714-725.
87. Ross, R.M. (1987) Sex-change linked growth acceleration in a coral-reef fish, Thalassoma duperrey. Journal of Experimental Zoology 244, 455-461.
88. Ross, R.M., Losey, G.S. and Diamond, M. (1983) Sex change in a coral reef fish: dependence of stimulation and inhibition of relative size. Science 221, 574-575.
89. Rubin, D.A. (1985) Effect of pH on sex ratio in cichlids and a poeciliid (Teleostei). Copeia 1985, 233-235.
90. Sadovy, Y. and Shapiro, D.Y. (1987) Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987, 136-156.
91. Seitz, A. (1942) Die Paarbildung bei einigen Cichliden II. Die Paarbildung bei Hemichromis bimaculatus (Gill). Zeitschrift für Tierpsychologie 5, 74-101.
92. Shapiro, D.Y. (1979) Social behaviour, group structure, and the control of sex reversal in hermaphroditic fish. In: Advances in the Study of Behaviour. Vol. 10 (eds J.S. Rosenblatt, R.A. Hinde, C. Beer and M.-C. Busnel). Academic Press, New York, pp. 43-102.
93. Shapiro, D.Y. (1987) Differentiation and evolution of sex change in fishes. Bioscience 37, 490-497.
94. Shapiro, D.Y. (1992) Plasticity of gonadal development and protandry in fishes. Journal of Experimental Zoology 261, 194-203.
95. Shapiro, D.Y. and Rasotto, M.B. (1993) Sex differentiation and gonadal development in the diandric, protogynous wrasse, Thalassoma bifasciatum (Pisces, Labridae). Journal of Zoology 230, 231-245.
96. Smith, C.L. (1975) The evolution of hermaphroditism in fishes. In: Intersexuality in the Animal Kingdom (ed. R. Reinboth). Springer-Verlag, Berlin, pp. 295-310.
97. Smith, C.L. and Young, P.H. (1966) Gonad structure and the reproductive cycle of the kelp bass, Paralabrax clathratus (Girard), with comments on the relationships of the serranid genus Paralabrax. California Fish and Game 52, 283-292.
98. Sparks, J.S. and Smith, W.L. (2004) Phylogeny and biogeography of cichlid fishes (Teleostei: Perciformes: Cichlidae). Cladistics 20, 501-517.
99. Stiassny, M.J.L. and Jensen, J.S. (1987) Labroid intrarelationships revisited: morphological complexity, key innovations, and study of comparative diversity. Bulletin of the Museum of Comparative Zoology 151, 269-319.
100. Streelman, J.T. and Karl, S.A. (1997) Reconstructing labroid evolution with single-copy nuclear DNA. Proceedings of the Royal Society of London B 264, 1011-1020.
101. Taborski, M. (1984) Broodcare helpers in Lamprologus brichardi: their costs and benefits. Animal Behaviour 32, 1236-1252.
102. Thompson, K.W. (1976) Some Aspects of Chromosomal Evolution of the Cichlidae (Teleostei: Perciformes) with Emphasis on Neotropical Forms. PhD thesis, University of Texas, Austin, TX, 132 pp.
103. Thresher, R.E. (1984) Reproduction in Reef Fishes. T.F.H. Publications, Neptune City, NJ, 399 pp.
104. Uchida, D., Yamashita, M., Kitano, T. and Iguchi, T. (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. Journal of Experimental Biology 205, 711-718.
105. Wang, L.H. and Tsai, C.L. (2000) Effects of temperature on the deformity and sex differentiation of Tilapia, Oreochromis mossambicus. Journal of Experimental Zoology 286, 534-537.
106. Ward, J.A. and Wyman, R.L. (1977) Ethology and ecology of cichlid fishes of the genus Etroplus in Sri Lanka: preliminary findings. Environmental Biology of Fishes 2, 137-145.
107. Warner, R.R. (1975) The adaptive significance of sequential hermaphroditism in animals. The American Naturalist 109, 61-82.
108. Warner, R.R. and Roberson, D.R. 1978. Sexual patterns in the Labroid fishes of the Western Caribbean, I: The wrasses (Labridae). Smithsonian Contributions to Zoology 254, 1-27.
109. Warner, R.R. and Swearer, S.E. (1991) Social control of sex change in the bluehead wrasse. Thalassoma bifasciatum (Pisces: Labridae). Biological Bulletin 181, 199-204.
110. Williams, N.J. (1972) On the Ontogeny of Behaviour of the Cichlid Fish Cichlasoma nigrofasciatum (Gunther). PhD Thesis, University of Groningen, The Netherlands, 112 pp.
111. Zhang, J. (2004) Evolution of DMY, a newly emergent male sex determination gene of medaka fish. Genetics 166, 1887-1895.
112. Zupanc, G.K.H. (1985) Fish and their Behaviour, How fishes Live: Specially Written for Aquarists. Tetra Press, Melle, Germany.