Evolutionary Ecology

, Volume 8, Issue 3, pp 256–268 | Cite as

The evolution of alternative mating strategies in variable environments

  • Jeffrey A. Hutchings
  • Ransom A. Myers


We assessed the influence of phenotypic plasticity in age at maturity on the maintenance of alternative mating strategies in male Atlantic salmon,Salmo salar. We calculated the fitness,r, associated with the parr and the anadromous strategies, using age-specific survival data from the field and strategy-specific fertilization data from the laboratory. The fitness of each strategy depended largely on mate competition (numbers of parr per female, i.e. parr frequency) and on age at maturity. Fitness declined with increasing numbers of parr per female with equilibrium frequencies (at which the fitnesses of each strategy are equal) being within the range observed in the wild. Equilibrium parr frequencies declined with decreasing growth rate and increasing age at maturity. Within populations, the existence of multiple age-specific sets of fitness functions suggests that the fitnesses of alternative strategies are best represented as multidimensional surfaces. The points of intersection of these surfaces, whose boundaries encompass natural variation in age at maturity and mate competition, define an evolutionarily stable continuum (ESC) of strategy frequencies along which the fitnesses associated with each strategy are equal. We propose a simple model that incorporates polygenic thresholds of a largely environmentally-controlled trait (age at maturity) to provide a mechanism by which an ESC can be maintained within a population. An indirect test provides support for the prediction that growth-rate thresholds for parr maturation exist and are maintained by stabilizing selection. Evolutionarily stable continua, maintained by negative frequency-dependent selection on threshold traits, provide a theoretical basis for understanding how alternative life histories can evolve in variable environments.


alternative mating strategies environmental variability life history evolution salmonid fish phenotypic plasticity 


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  1. Alm, G. (1959) Connection between maturity, size, and age in fishes.Rep. Inst. Freshwater Res., Drottningholm 40 1–145.Google Scholar
  2. Ash, E.G.M. and O'Connell, M.F. (1987) Atlantic salmon fishery in Newfoundland and Labrador, commercial and recreational, 1985.Can. Data Rep. Fish. Aquat. Sci. No. 672 284.Google Scholar
  3. Berglund, I., Schmitz, M. and Lundqvist, H. (1992) Seawater adaptability in Baltic salmon (Salmo salar): a bimodal smoltification pattern in previously mature males.Can. J. Fish. Aquat. Sci. 49 1097–106.Google Scholar
  4. Bley, P.W. and Moring, J.R. (1988) Freshwater and ocean survival of Atlantic salmon and steelhead: a synopsis.US Fish Wildl. Serv. Biol. Rep. 91, 88–109.Google Scholar
  5. Bohlin, T., Dellefors, C. and Faremo, U. (1990) Large or small at maturity — theories on the choice of alternative male strategies in anadromous salmonids.Ann. Zool. Fenn. 27 139–47.Google Scholar
  6. Bradshaw, A.D. (1965) Evolutionary significance of phenotypic plasticity in plants.Adv. Genet. 13 115–55.Google Scholar
  7. Falconer, D.S. (1989)Introduction to Quantitative Genetics. Longman, London.Google Scholar
  8. Field-Dodgson, M.J. (1988) Size characteristics and diet of emergent chinook salmon in a small, stable, New Zealand stream.J. Fish Biol. 32 27–40.Google Scholar
  9. Gavrilets, S. and Scheiner, S.M. (1993) The genetics of phenotypic plasticity. V. Evolution of reaction norm shape.J. Evol. Biol. 6 31–48.Google Scholar
  10. Gibson, R.J., Porter, T.R. and Hillier, K.G. (1987) Juvenile salmonid production in the Highlands River, St. George's Bay, Newfoundland.Can. Tech. Rep. Fish. Aquat. Sci. No. 1538.Google Scholar
  11. Gross, M.R. (1985) Disruptive selection for alternative life histories in salmon.Nature 313 47–8.Google Scholar
  12. Gross, M.R. (1991a) Evolution of alternative strategies: frequency-dependent sexual selection in male bluegill sunfish.Phil. Trans. R. Soc. Lond. B 332 59–66.Google Scholar
  13. Gross, M.R. (1991b) Salmon breeding behavior and life history evolution in changing environments.Ecology 72 1180–6.Google Scholar
  14. Hazel, W.N., Smock, R. and Johnson, M.D. (1990) A polygenic model for the evolution and maintenance of conditional strategies.Proc. R. Soc. Lond. B 242 181–7.Google Scholar
  15. Houston, A.I. and McNamara, J.M. (1992) Phenotypic plasticity as a state-dependent life-history decision.Evol. Ecol. 6 243–53.Google Scholar
  16. Hutchings, J.A. (1985) The adaptive significance of lakeward migrations by juvenile Atlantic salmon,Salmo salar Linnaeus. MSc dissertation Memorial University of Newfoundland, St John's, Canada.Google Scholar
  17. Hutchings, J.A. (1993a) Adaptive life histories effected by age-specific survival and growth rate.Ecology 74 673–84.Google Scholar
  18. Hutchings, J.A. (1993b) Reaction norms for reproductive traits in brook trout and their influence on life history evolution effected by size-selective harvesting. InThe exploitation of evolving resources (T.K. Stokes, J.M. McGlade and R. Law, eds), pp. 107–125, Springer-Verlag, Berlin.Google Scholar
  19. Hutchings, J.A. and Morris, D.W. (1985) The influence of phylogeny, size and behaviour on patterns of covariation in salmonid life histories.Oikos 45 118–24.Google Scholar
  20. Hutchings, J.A. and Myers, R.A. (1986) The economics of artificial selection for reducing the proportion of mature male parr in natural populations of Atlantic salmon,Salmo salar. Int. Counc. Explor. Sea CM Mini-Symposium,3, 25 pps.Google Scholar
  21. Hutchings, J.A. and Myers, R.A. (1988) Mating success of alternative maturation phenotypes in male Atlantic salmon,Salmo salar.Oecologia 75 169–74.Google Scholar
  22. Jones, J.W. (1959)The Salmon. Collins, London.Google Scholar
  23. Jordan, W.C. and Youngson, A.F. (1992) The use of genetic marking to assess the reproductive success of mature male Atlantic salmon parr (Salmo salar, L.) under natural spawning conditions.J. Fish Biol. 41 613–18.Google Scholar
  24. Kawecki, T.J. and Stearns, S.C. (1993) The evolution of life histories in spatially heterogeneous environments: optimal reaction norms revisited.Evol. Ecol. 7 155–74.Google Scholar
  25. Leonardsson, K. and Lundberg, P. (1986) The choice of reproductive tactics as a mixed evolutionarily stable strategy: the case of male Atlantic salmon (Salmo salar L.).Rep. Inst. Freshwater Res., Drottningholm 63 69–76.Google Scholar
  26. Levins, R. (1968)Evolution in Changing Environments. Princeton University Press, Princeton, NJ.Google Scholar
  27. Maynard Smith, J. (1982)Evolution and the Theory of Games. Cambridge University Press, Cambridge.Google Scholar
  28. Metcalfe, N.B., Wright, P.J. and Thorpe, J.E. (1992) Relationships between social status, otolith size at first feeding and subsequent growth in Atlantic salmon (Salmo salar).J. Anim. Ecol. 61 585–9.Google Scholar
  29. Murray, A.R. (1968) Smolt survival and adult utilization of Little Codroy River, Newfoundland, Atlantic salmon.J. Fish. Res. Board Can. 25 2165–218.Google Scholar
  30. Myers, R.A. (1984) Demographic consequences of precocious maturation of Atlantic salmon (Salmo salar).Can. J. Fish. Aquat. Sci. 41 1349–53.Google Scholar
  31. Myers, R.A. (1986) Game theory and the evolution of Atlantic salmon (Salmo salar) age at maturation.Can. Spec. Publ. Fish. Aquat. Sci. 89 53–61.Google Scholar
  32. Myers, R.A. and Hutchings, J.A. (1986) Selection against parr maturation in Atlantic salmon.Aquaculture 53 313–20Google Scholar
  33. Myers, R.A. and Hutchings, J.A. (1987) Mating of anadromous Atlantic salmon,Salmo salar, with mature male parr.J. Fish Biol. 32 143–6.Google Scholar
  34. Myers, R.A., Hutchings, J.A. and Gibson, R.J. (1986) Variation in male parr maturation within and among populations of Atlantic salmon,Salmo salar.Can. J. Fish. Aquat. Sci. 43 1242–8.Google Scholar
  35. Naevdal, G., Holm, M., Moller, D. and Osthus, O.D. (1976) Variation in growth rate and age at sexual maturity in Atlantic salmon.Int. Counc. Explor. Sea CM E: 40.Google Scholar
  36. Needham, A.E. (1964)The Growth Process in Animals. Pitman, London.Google Scholar
  37. Northcote, T.G. (1984) Mechanisms of fish migration in rivers. InMechanisms of migration in fishes (J.D. McCleave, G.P. Arnold, J.J. Dodson and W.H. Neill, eds), pp. 317–55. Plenum Press, New York.Google Scholar
  38. Parker, G.A. (1984) Evolutionarily stable strategies. InBehavioural ecology: an evolutionary approach (J.R. Krebs, and N.B. Davies, eds), pp. 30–61. Blackwell, Sunderland, MA.Google Scholar
  39. Partridge, L. (1988) The rare-male effect: what is its evolutionary significance?Phil. Trans. R. Soc. Lond. B 319 525–39.Google Scholar
  40. Power, G. (1980) The brook charr,Salvelinus fontinalis. InCharrs: salmonid fishes of the genus Salvelinus (E.K. Balon, ed.), pp. 141–203. Dr W. Junk, The Hague, Netherlands.Google Scholar
  41. Ricker, W.E. (1975) Computation and interpretation of biological statistics of fish populations.Fish. Res. Board Can. Bull. 191 Google Scholar
  42. Schaffer, W.M. (1974) Selection for optimal life histories: the effects of age structure.Ecology 55 291–303.Google Scholar
  43. Schmalhausen, I.I. (1949)Factors of Evolution. Blakiston, Philadelphia.Google Scholar
  44. Slatkin, M. (1978) On the equilibration of fitnesses by natural selection.Am. Nat. 112 845–59.Google Scholar
  45. Snucins, E.J., Curry, R.A. and Gunn, J.M. (1992) Brook trout (Salvelinus fontinalis) embryo habitat and timing of alevin emergence in a lake and a stream.Can. J. Zool. 70 423–7.Google Scholar
  46. Stearns, S.C. and Koella, J. (1986) The evolution of phenotypic plasticity in life-history traits: predictions for norms of reaction for age- and size-at-maturity.Evolution 40, 893–913.Google Scholar
  47. Thorpe, J.E. (1986) Age at first maturity in Atlantic salmon,Salmo salar: freshwater period influences and conflicts with smolting.Can. Spec. Pub. Fish. Aquat. Sci. 89 7–14.Google Scholar
  48. Thorpe, J.E., Morgan, R.I.G., Talbot, C. and Miles, M.S. (1983) Inheritance of developmental rates in Atlantic salmon,Salmo salar L.Aquaculture 33 119–28.Google Scholar
  49. van den Berghe, E.P. and Gross, M.R. (1989) Natural selection resulting from female breeding competition in a Pacific salmon (coho:Oncorhynchus kisutch).Evolution 43 125–40.Google Scholar
  50. Via, S. and Lande, R. (1985) Genotype-environment interaction and the evolution of phenotypic plasticity.Evolution 39, 505–22.Google Scholar

Copyright information

© Chapman & Hall 1994

Authors and Affiliations

  • Jeffrey A. Hutchings
    • 1
  • Ransom A. Myers
    • 2
  1. 1.Institute of Cell, Animal and Population BiologyUniversity of EdinburghEdinburghUK
  2. 2.Science BranchDepartment of Fisheries and OceansSt John'sCanada

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