Sex change as an alternative life-history style

  • Douglas Y. Shapiro
Part of the Perspectives in vertebrate science book series (PIVS, volume 6)


The proximate mechanism controlling the initiation of sex change tunes the timing of sex change to particular behavioral and demographic alterations within the social system. Consequently, changes from one sex to another are condition-dependent. A number of aspects of sex-changing species might be considered alternatives depending on our definition of alternative tactics and the level of analysis desired. Theoretical approaches to sex change as an alternative life-history tactic should address the issue of intrapopulational variation in the timing of sex change. A model by Caswell (1983) can be applied to this question. The result is a new explanation for early sex change. Alternative male spawning patterns in diandric species require the existence of alternative female spawning behaviors. When the spawning system is viewed from the female perspective, a new explanation emerges for the increase in reproductive success with increasing reef size observed in initial phase males of one diandric fish.

Key words

Fishes Condition-dependent Plasticity Behavior Demography Spawning Reproductive success Reef size 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aldenhoven, J.M. 1984. Social organization and sex change in an angelfish ‘Centropyge bicolor’ on the Great Barrier Reef. Ph.D. Thesis, Macquarie University, North Ryde. 214 pp.Google Scholar
  2. Aldenhoven, J.M. 1986. Different reproductive strategies in a sex-changing coral reef fish’ Centropyge bicolof (Pomacanthidae). Aust. J. Mar. Freshw. Res. 37: 353–360.CrossRefGoogle Scholar
  3. Buxton, C.D. & P.A. Garratt. 1989. Alternative reproductive styles in seabreams (Pisces: Sparidae). Env. Biol. Fish, (in press).Google Scholar
  4. Cade, W. 1979. The evolution of alternative male reproductive strategies in field crickets. pp. 343–379. In: M.S. Blum & N.A. Blum (ed.) Sexual Selection and Reproductive Competition in Insects, Academic Press, New York.Google Scholar
  5. Caro, T.M. & P. Bateson. 1986. Organization and ontogeny of alternative tactics. Anim. Behav. 34: 1483–1499.CrossRefGoogle Scholar
  6. Caswell, H. 1983. Phenotypic plasticity in life-history traits: demographic effects and evolutionary consequences. Amer. Zool. 23: 35–46.Google Scholar
  7. Chan, S.T.H. & W.S.B. Yeung. 1983. Sex control and sex reversal in fish under natural conditions, pp. 171–222. In: W.S. Hoar, D.J. Randall & E.M. Donaldson (ed.) Fish Physiology, Vol. 9, Reproduction, B: Behavior and Fertility Control, Academic Press, New York.Google Scholar
  8. Charnov, E.L. 1982. Alternative life histories in protogynous fishes: a general evolutionary theory. Mar. Ecol. Prog. Ser. 9: 305–307.CrossRefGoogle Scholar
  9. Charnov, E.L. 1986. Size advantage may not always favor sex change. J. Theor. Biol. 119: 283–285.PubMedCrossRefGoogle Scholar
  10. Clavijo, I. 1982. Aspects of the reproductive biology of the redband parrotfish ‘Sparisoma aurofrenatum’. Ph.D. Thesis, University of Puerto Rico, Mayaguez. 151 pp.Google Scholar
  11. Dominey, W.J. 1980. Female mimicry in male bluegill sunfish — a genetic polymorphism? Nature (Lond.) 284: 546–548.CrossRefGoogle Scholar
  12. Dominey, W.J. 1984. Alternative mating tactics and evolutionary stable strategies. Amer. Zool. 24: 385–396.Google Scholar
  13. Dunbar, R.I.M. 1982. Intraspecific variations in mating strategy, pp. 385–431. In: P.P.G. Bateson & R.H. Klopfer (ed.) Perspectives in Ethology 5: Ontogeny, Plenum Press, New York.Google Scholar
  14. Fishelson, L. 1970. Protogynous sex reversal in the fish Anthias squamipinnis (Teleostei, Anthiidae) regulated by the presence or absence of a male fish. Nature (Lond.) 227: 90–91.Google Scholar
  15. Fricke, H.W. 1979. Mating systems, resource defense and sex change in the anemonefish Amphiprion akallopisos. Z. Tierpsychol. 50: 313–326.CrossRefGoogle Scholar
  16. Fricke, H.W. 1983. Social control of sex: field experiments with the anemonefish Amphiprion bicinctus. Z. Tierpsychol. 61: 71–77.Google Scholar
  17. Fricke, H.W. & S. Fricke. 1977. Monogamy and sex change by aggressive dominance in a coral reef fish. Nature (Lond.) 266: 830–832.PubMedCrossRefGoogle Scholar
  18. Ghiselin, M.T. 1969. The evolution of hermaphroditism among animals. Quart. Rev. Biol. 44: 189–208.PubMedCrossRefGoogle Scholar
  19. Gross, M.R. & E.L. Charnov. 1980. Alternative male life histories in bluegill sunfish. Proc. Nat. Acad. Sci. USA 77: 6937–6940.PubMedCrossRefGoogle Scholar
  20. Hoffman, S.G. 1983. Sex-related foraging behavior in sequentially hermaphroditic hogfishes (Bodianus spp.). Ecology 64: 798–808.CrossRefGoogle Scholar
  21. Hoffman, S.G., M.R Schildhauer & R.R. Warner. 1985. The costs of changing sex and the ontogeny of males under contest competition for mates. Evolution 39: 915–927.CrossRefGoogle Scholar
  22. Hogan-Warburg, A.J. 1966. Social behavior of the ruff, Philomachus pugnax (L.). Ardea 54: 109–222.Google Scholar
  23. Howard, R.D. 1984. Alternative mating behaviors of young male bullfrogs. Amer. Zool. 24: 397–406.Google Scholar
  24. Krebs, J.R. & N.B. Davies. 1981. An introduction to behavioural ecology. Sinauer Associates, Sunderland. 291 pp.Google Scholar
  25. Moyer, J.T. & M.J. Zaiser. 1984. Early sex change: a possible mating strategy of Centropyge angelfishes (Pisces: Pomacanthidae). J. Ethol. 2: 63–67.CrossRefGoogle Scholar
  26. Pechan, P., D.Y. Shapiro & M. Tracey. 1986. Increased H-Y antigen levels associated with behaviorally-induced, female-to-male sex reversal in a coral-reef fish. Differentiation 31: 106–110.PubMedCrossRefGoogle Scholar
  27. Policansky, D. 1981. Sex choice and the size advantage model in Jack-in-the-Pulpit (Arisaema triphyllum). Proc. Nat. Acad. Sci. USA 78: 1306–1308.PubMedCrossRefGoogle Scholar
  28. Popper, D. & L. Fishelson. 1973. Ecology and behavior of Anthias squamipinnis (Peters, 1855) (Anthiidae, Teleostei) in the coral habitat of Eilat (Red Sea). J. Exp. Zool. 184: 409–424.CrossRefGoogle Scholar
  29. Reinboth, R. 1962. Morphologische und funktionelle Zweigeschlechtigkeit bei marinen Teleostiern (Serranidae, Sparidae, Centracanthidae, Labridae). Zool. Jahrb. Abt. Allg. Zool. Physiol. Tiere 69: 405–480.Google Scholar
  30. Reinboth, R. 1967. Biandric teleost species. Gen. Comp. Endocrinol. 9: 486.Google Scholar
  31. Reinboth, R. 1970. Intersexuality in fishes. Mem. Soc. Endocrinol. 18: 515–543.Google Scholar
  32. Reinboth, R. 1973. Dualistic reproductive behavior in the protogynous wrasse Thalassoma bifasciatum and some observations on its day-night changeover. Helgol. wiss. Meeresunters. 24: 174–191.Google Scholar
  33. Robertson, D.R. 1972. Social control of sex-reversal in a coral-reef fish. Science 177: 1007–1009.PubMedCrossRefGoogle Scholar
  34. Robertson, D.R. 1973. Sex change under the waves. New Scientist 58: 538–540.Google Scholar
  35. Robertson, D.R. & S.G. Hoffman. 1977. The roles of female mate choice and predation in the mating systems of some tropical labroid fishes. Z. Tierpsychol. 45: 298–320.Google Scholar
  36. Roede, M.J. 1972. Color as related to size, sex, and behaviour in seven Caribbean labrid fish species (genera Thalassoma, Halichoeres, Hemipteronotus). Stud. Fauna Curacao a.o. Carib. Islands 42: 1–264.Google Scholar
  37. Ross, R.M., G.S. Losey & M. Diamond. 1983. Sex change in a coral-reef fish: dependence of stimulation and inhibition on relative size. Science 221: 574–575.PubMedCrossRefGoogle Scholar
  38. Rubinstein, D.I. 1980. On the evolution of alternative mating strategies, pp. 65–100. In: J.E.R. Staddon (ed.) Limits to Action: The Allocation of Individual Behavior, Academic Press, New York.Google Scholar
  39. Rubinstein, D.I. 1984. Resource acquisition and alternative mating strategies in water striders. Amer. Zool. 24: 345–353.Google Scholar
  40. Sabat, A. 1985. Use of space in relation to the regulation of social interactions in the protogynous hermaphrodite ‘Anthias squamipinnis’. M.Sc. Thesis, University of Puerto Rico, Mayaguez. 83 pp.Google Scholar
  41. Sadovy, Y. & D.Y. Shapiro. 1987. Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987: 136–156.CrossRefGoogle Scholar
  42. Sale, RF. 1984. The structure of communities of fish on coral reefs and the merit of a hypothesis-testing, manipulative approach to ecology, pp. 478–490. In: D.R. Strong, Jr., D. Simberloff, L.G. Abele & A.B. Thistle (ed.) Ecological Communities: Conceptual Issues and the Evidence, Princeton University Press, Princeton.Google Scholar
  43. Shapiro, D.Y. 1979. Social behavior, group structure and the control of sex reversal in hermaphroditic fish. Adv. Study Behav. 10: 43–102.CrossRefGoogle Scholar
  44. Shapiro, D.Y. 1981a. Size, maturation and the social control of sex reversal in the coral reef fish Anthias squamipinnis (Peters), J. Zool. 193: 105–128.CrossRefGoogle Scholar
  45. Shapiro, D.Y. 1981b. The sequence of coloration changes during sex reversal in the tropical marine fish Anthias squamipinnis (Peters). Bull. Mar. Sci. 31: 383–398.Google Scholar
  46. Shapiro, D.Y. 1983. Distinguishing direct behavioral interactions from visual cues as causes of adult sex change in a coral reef fish. Horm. Behav. 17: 424–433.PubMedCrossRefGoogle Scholar
  47. Shapiro, D.Y. 1984. Sex reversal and sociodemographic processes in coral reef fishes, pp. 103–118. In: G.W. Potts & R.J. Wootton (ed.) Fish Reproduction: Strategies and Tactics, Academic Press, London.Google Scholar
  48. Shapiro, D.Y. 1987. Differentiation and evolution of sex change in fishes. BioSci. 37: 490–497.CrossRefGoogle Scholar
  49. Shapiro, D.Y. 1988. Behavioral influences on gene structure and other new ideas concerning sex change in fishes. Env. Biol. Fish. 23: 283–297.CrossRefGoogle Scholar
  50. Shapiro, D.Y. & R. Boulon. 1982. The influence of females on the initiation of femaleto-male sex change in a coral reef fish. Horm. Behav. 16: 66–75.PubMedCrossRefGoogle Scholar
  51. Shapiro, D.Y. & R. Lubbock. 1980. Group sex ratio and sex reversal. J. Theor. Biol. 82: 411–426.Google Scholar
  52. Thornhill, R. 1981. Panorpa (Mecoptera: Panorpidae) scorpionflies: systems for understanding resource-defense polygyny and alternative reproductive efforts. Ann. Rev. Ecol. Syst. 12: 355–386.CrossRefGoogle Scholar
  53. Thornhill, R. 1984. Alternative female choice tactics in the scorpionfly Hylobittacus apicalis (Mecoptera) and their implications. Amer. Zool. 24: 367–383.Google Scholar
  54. Victor, B.C. 1986. Larval settlement and juvenile mortality in a recruitment-limited coral reef fish population. Ecol. Monogr. 56: 145–160.CrossRefGoogle Scholar
  55. Waltz, E.C. & L.L. Wolf. 1984. By Jove!! Why do alternative mating tactics assume so many different forms? Amer. Zool. 24: 333–343.Google Scholar
  56. Warner, R.R. 1984. Deferred reproduction as a response to sexual selection in a coral reef fish: a test of the life historical consequences. Evolution 38: 148–162.CrossRefGoogle Scholar
  57. Warner, R.R. 1988. Sex change in fishes: hypotheses, evidence, and objections. Env. Biol. Fish. 22: 81–90.CrossRefGoogle Scholar
  58. Warner, R.R. & S.G. Hoffman. 1980a. Population density and the economics of territorial defense in a coral reef fish. Ecology 61: 772–780.CrossRefGoogle Scholar
  59. Warner, R.R. & S.G. Hoffman. 1980b. Local population size as a determinant of mating system and sexual composition in two tropical marine fishes (Thalassoma spp.). Evolution 34:508–518.CrossRefGoogle Scholar
  60. Warner, R.R. & D.R. Robertson. 1978. Sexual patterns in the labroid fishes of the western Caribbean: I. The wrasses (Labridae). Smithson. Contrib. Zool. 254: 1–27.CrossRefGoogle Scholar
  61. Warner, R.R., D.R. Robertson & E.G. Leigh. 1975. Sex change and sexual selection. Science 190: 633–638.PubMedCrossRefGoogle Scholar
  62. Wood, E.M. 1981. Sex change and other social strategies in anemonefish. Prog. Underwater Sci. 6: 61–64.Google Scholar
  63. Wood, E.M. 1986. Behavior and social organization in anemonefish. Prog. Underwater Sci. 11: 53–60.Google Scholar
  64. Yeung, W.S.B. & S.T.H. Chan. 1987a. The plasma sex steroid profiles in the freshwater, sex-reversing teleost fish, Monopterus albus (Zuiew). Gen. Comp. Endocrinol. 65: 233–242.CrossRefGoogle Scholar
  65. Yeung, W.S.B. & S.T.H. Chan. 1987b. A radioimmunoassay study of the plasma levels of sex steroids in the protandrous, sex-reversing fish Rhabdosargus sarba (Sparidae). Gen. Comp. Endocrinol. 66: 353–363.CrossRefGoogle Scholar
  66. Yogo, Y 1986. Protogyny, reproductive behavior and social structure of the Anthiine fish Anthias (Franzia) squamipinnis. p. 964. In: T. Uyeno, R. Arai, T. Taniuchi & K. Matsuura (ed.) Indo-Pacific Fish Biology, The Ichthyological Society of Japan, Tokyo.Google Scholar

Copyright information

© Kluwer Academic Publishers, Dordrecht 1989

Authors and Affiliations

  • Douglas Y. Shapiro
    • 1
  1. 1.Department of Marine SciencesUniversity of Puerto RicoMayaguez, Puerto RicoUSA

Personalised recommendations