Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.)

Evolution

Volumn 57, Issue 5, 2003, Pages 1133-1141

  Garant, Dany ^a   Dodson, Julian J ^a   Bernatchez, Louis ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Alternative strategy; Environmental effects; Fitness; Juvenile growth; Salmonidae

Indexed keywords

ENVIRONMENTAL EFFECT; EVOLUTION; FITNESS; GENOTYPE; HERITABILITY; JUVENILE; LIFE HISTORY; REPRODUCTIVE SUCCESS; SALMONID;

ANIMALIA; SALMO; SALMO SALAR; SALMONIDAE; VERTEBRATA;

EID: 0038311037     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2003.tb00322.x     Document Type: Article

References (91)

1. Anderson, T. C. 1985. The rivers of Labrador. Can. Spec. Pub. Fish. Aquat. Sci. 81:1-389.
2. Avise, J. C. 2001. DNA-based profiling of genetic mating systems and reproductive behaviors in poikilothermic vertebrates. J. Hered. 92:99-211.
3. Belding, D. L. 1934. The spawning habits of the Atlantic salmon. Trans. Am. Fish. Soc. 64:211-218.
4. Berglund, I. 1992. Growth and early sexual maturation in Baltic salmon (Salmo salar) parr. Can. J. Zool. 70:205-211.
5. Bernatchez, L., and P. Duchesne. 2000. Individual-based genotype analysis in studies of parentage and population assignment: how many loci, how many alleles? Can. J. Fish. Aquat. Sci. 57:1-12.
6. Bernatchez, L., R. Guyomard, and F. Bonhomme. 1992. DNA sequence variation of the mitochondrial control region among geographically and morphologically remote European brown trout Salmo trutta populations. Mol. Ecol. 1:161-173.
7. Bohlin, T., C. Dellefors, and U. Faremo. 1990. Large or small at maturity - theories on the choice of alternative male strategies in anadromous salmonids. Ann. Zool. Fenn. 27:139-147.
8. Brockmann, H. J., 2001. The evolution of alternative strategies and tactics. Adv. Study Behav. 30:1-51.
9. Brockmann, H. J., T. Colson, and W. Potts. 1994. Sperm competition in horseshoe crabs (Limulus polyphemus). Behav. Ecol. Sociobiol. 35:153-160.
10. Chadwick, E. M. P., R. G. Randall, and C. Léger. 1986. Ovarian development of Atlantic salmon (Salmo salar) smolts and age at first maturity. Can. Spec. Pub. Fish. Aquat. Sci. 89:15-23.
11. Clutton-Brock, T. H. 1988. Reproductive success. Univ. of Chicago Press, Chicago, IL.
12. Coltman, D. W., D. R. Bancroft, A. Robertson, J. A. Smith, T. H. Clutton-Brock, and J. M. Pemberton. 1999. Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol. Ecol. 8:1199-1209.
13. Crespi, B. J. 1988. Alternative male mating tactics in a thrips: effects of sex ratio variation and body size. Am. Midl. Nat. 119:83-92.
14. Crisp, D. T. 1995. Dispersal and growth of 0-group salmon (Salmo salar L.) from point stocking together with some information from scatter stocking. Ecol. Freshw. Fish 4:1-8.
15. Dhondt, A. A. 1982. Heritability of blue tit tarsus length from normal and cross-fostered broods. Evolution 36:418-419.
16. Duchesne, P., M.-H. Godbout, and L. Bernatchez. 2002. PAPA (Package for the analysis of parental allocation): a computer program for simulated and real parental allocation. Mol. Ecol. Notes 2:191-193.
17. Einum, S., and I. A. Fleming. 1999. Maternal effects of egg size in brown trout (Salmo trutta): norm of reaction to environmental quality. Proc. R. Soc. Lond. B 266:2095-2100.
18. _. 2000. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54:628-639.
19. Erkinaro, J., and E. Niemelä. 1995. Growth differences between the Atlantic salmon parr, Salmo salar, of nursery brooks and natal rivers in the River Teno watercourse in northern Finland. Environ. Biol. Fish. 42:277-287.
20. Falconer, D. S. 1989. Introduction to quantitative genetics. Longman, London.
21. Fleming, I. A. 1998. Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can. J. Fish. Aquat. Sci. 55:59-76.
22. Foote, C. J., G. S. Brown, and C. C. Wood. 1997. Spawning success of males using alternative mating tactics in sockeye salmon, Oncorhynchus nerka. Can. J. Fish. Aquat. Sci. 54:1785-1795.
23. Friedland, K. D., and R. E. Haas. 1996. Marine post-smolt growth and age at maturity of Atlantic salmon. J. Fish Biol. 48:1-15.
24. Garant, D., J. J. Dodson, and L. Bernatchez. 2000. Ecological determinants and temporal stability of within-river population structure in Atlantic salmon (Salmo salar L.). Mol. Ecol. 9:615-628.
25. _. 2001. A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). J. Hered. 92:137-145.
26. Garant, D., P.-M. Fontaine, S. P. Good, J. J. Dodson, and L. Bernatchez. 2002. Influence of male parental identity on growth and survival of offspring in Atlantic salmon (Salmo salar). Evol. Ecol. Res. 4:537-549.
27. Gibbs, H. L., P. J. Weatherhead, P. T. Boag, B. N. White, L. M. Tabak, and D. J. Hoysak. 1990. Realized reproductive success of polygynous red-winged blackbirds revealed by DNA markers. Science 250:1394-1398.
28. Glebe, B. D., and R. L. Saunders. 1986. Genetic factors in sexual maturity of cultured Atlantic salmon (Salmo salar) parr and adults reared in sea cages. Can. Spec. Pub. Fish. Aquat. Sci. 89:24-29.
29. Gross, M. R. 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11:92-98.
30. Gross, M. R., and J. Repka. 1998a. Game theory and inheritance in the conditional strategy. Pp. 168-187 in L.A. Dugatkin, and H.K. Reeve, eds. Game theory and animal behavior. Oxford Univ. Press, Oxford, U.K.
31. _. 1998b. Stability with inheritance in the conditional strategy. J. Theor. Biol. 192:445-453.
32. Hazel, W. N., R. Smock, and M. D. Johnson. 1990. A polygenic model for the evolution and maintenance of conditional strategies. Proc. R. Soc. Lond. B 242:181-187.
33. Hazel, W. N., and R. Smock. 1993. Modeling selection on conditional strategies in stochastic environment. Pp. 147-154 in J. Yoshimura, and C.W. Clark, eds. Lecture notes in biomathematics: Adaptation in stochastic environments. Springer, Berlin.
34. Heath, D. D., C. W. Fox, and J. W. Heath. 1999. Maternal effects on offspring size: variation through early development of chinook salmon. Evolution 53:1605-1611.
35. Hofmann, H. A., M. E. Benson, and R. D. Fernald. 1999. Social status regulates growth rate: consequences for life-history strategies. Proc. Natl Acad. Sci. USA 96:14171-14176.
36. Hunt, J., and L. W. Simmons. 2000. Maternal and paternal effects on offspring phenotype in the dung beetle Ontophagus taurus. Evolution 54:936-941.
37. _. 2001. Status-dependent selection in the dimorphic beetle Ontophagus taurus. Proc. R. Soc. Lond. B 268:2409-2414.
38. Hutchings, J. A., and M. E. B. Jones. 1998. Life history variation and growth rate thresholds for maturity in Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci. 55(Suppl. 1):22-47.
39. Hutchings, J. A., and R. A. Myers. 1994. The evolution of alternative mating strategies in variable environments. Evol. Ecol. 8:256-268.
40. Jonasson, J. 1993. Selection experiments in salmon ranching. I. Genetic and environmental sources of variation in survival and growth in freshwater. Aquaculture 109:225-236.
41. Jones, J. W., and J. N. Ball. 1954. The spawning behaviour of brown trout and salmon. Br. J. Anim. Behav. 2:103-114.
42. Kazakov, R. V. 1981. The effect of the size of Atlantic salmon, Salmo salar L., eggs on embryos and alevins. J. Fish Biol. 19:353-360.
43. Keeley, E. R., and J. W. A. Grant. 2001. Prey size of salmonid fishes in streams, lakes, and oceans. Can. J. Fish. Aquat. Sci. 58:1122-1132.
44. Knott, S. A., R. M. Sibly, R. H. Smith, and H. Møller. 1995. Maximum likelihood estimation of genetic parameters in life-history studies using the "animal model." Funct. Ecol. 9:122-126.
45. Kruuk, L. E. B., T. H. Clutton-Brock, J. Slate, J. M. Pemberton, S. Brotherstone, and F. E. Guinness. 2000. Heritability of fitness in a wild mammal population. Proc. Natl Acad. Sci. USA 97:698-703.
46. Lank, D. B., C. M. Smith, O. Hanotte, T. Burke, and T. Cooke. 1995. Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62.
47. Larsson, K., K. Rattiste, and V. Lilleleht. 1997. Heritability of head size in the common gull Larus canus in relation to environmental conditions during offspring growth. Heredity 79:201-207.
48. Lundqvist, H. 1980. Influence of photoperiod on growth in Baltic salmon parr (Salmo salar L.) with special reference to the effect of precocious sexual maturation. Can. J. Zool. 58:940-944.
49. Maynard Smith, J. 1982. Evolution and the theory of games. Cambridge Univ. Press, Cambridge, U.K.
50. McCormick, S. D., L. P. Hansen, T. P. Quinn, and R. L. Saunders. 1998. Movement, migration, and smolting of Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 55(Suppl. 1):77-92.
51. Merilä, J. 1997. Expression of genetic variation in body size of the collared flycatcher under different environmental conditions. Evolution 51:526-536.
52. Merilä, J., and J. D. Fry. 1998. Genetic variation and causes of genotype-environment interaction in the body size of blue tit (Parus caeruleus). Genetics 148:1233-1244.
53. Merilä, J., L. E. B. Kruuk, and B. C. Sheldon. 2001. Natural selection on the genetical component of variance in body condition in a wild bird population. J. Evol. Biol. 14:918-929.
54. Meyer, K. 1989. Restricted maximum likelihood to estimate variance components for animal models with several random effects using a derivative-free algorithm. Genet. Sel. Evol. 23:67-83.
55. _. 1998. DFREML 3.0. Available via the DFREML home page: http://agbu.une.edu.au/~kmeyer/dfreml.html.
56. Milner, J. M., J. M. Pemberton, S. Brotherstone, and S. D. Albon. 2000. Estimating variance components and heritabilities in the wild: a case study using the "animal model" approach. J. Evol. Biol. 13:804-813.
57. Moczek, A. P., and D. J. Emlen. 1999. Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J. Evol. Biol. 12:27-37.
58. Mousseau, T. A., and D. A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181-197.
59. Mousseau, T. A., and C. W. Fox. 1998. Maternal effects as adaptations. Oxford Univ. Press, New York.
60. Myers, R. A. 1984. Demographic consequences of precocious maturation of Atlantic salmon (Salmo salar). Can. J. Fish. Aquat. Sci. 41:1349-1353.
61. Myers, R. A., J. A. Hutchings, and R. J. Gibson. 1986. Variation in male parr maturation within and among populations of Atlantic salmon, Salmo salar. Can. J. Fish. Aquat. Sci. 43:1242-1248.
62. Naevdal, G. 1983. Genetic factors in connection with age at maturation. Aquaculture 33:97-106.
63. Naevdal, G., M. Holm, D. Møller, and O. D. Osthus. 1976. Variation in growth rate and age at sexual maturity in Atlantic salmon. Int. Counc. Explor. Sea 1976/E:40.
64. Nager, R. G., L. F. Keller, and A. J. Van Noordwijk. 2000. Understanding natural selection on traits that are affected by environmental conditions. Pp. 95-115 in T. A. Mousseau, B. Sinervo, and J. A. Endler, eds. Adaptive genetic variation in the wild. Oxford Univ. Press, New York.
65. Naiman, R. J., J. M. Melillo, M. A. Lock, T. E. Ford, and S. R. Reice. 1987. Longitudinal patterns of ecosystem processes and community structure in a subarctic river continuum. Ecology 68:1139-1156.
66. O'Reilly, P. T., L. C. Hamilton, S. K. McConnell, and J. M. Wright. 1996. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci. 53:2292-2298.
67. Pakkasmaa, S., N. Peuhkuri, A. Laurila, H. Hirvonen, and R. Ranta. 2001. Female and male contribution to egg size in salmonids. Evol. Ecol. 15:143-153.
68. Presa, P., and R. Guyomard. 1996. Conservation of microsatellites in three species of salmonids. J. Fish Biol. 49:1326-1329.
69. Qvarnström, A. 1999. Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher (Ficedula albicollis). Evolution 53:1564-1572.
70. Qvarnström, A., and T. Price. 2001. Maternal effects, paternal effects and sexual selection. Trends Ecol. Evol. 16:95-100.
71. Radwan, J. 1995. Male morph determination in two species of acarid mites. Heredity 74:669-673.
72. Réale, D., M. Festa-Bianchet, and J. T. Jorgenson. 1999. Heritability of body mass varies with age and season in wild bighorn sheep. Heredity 83:526-532.
73. Ritland, K. 2000. Marker-inferred relatedness as a tool for detecting heritability in nature. Mol. Ecol. 9:1195-1204.
74. Ritter, J. A., G. J. Farmer, R. K. Misra, T. R. Goff, J. K. Bailey, and E. T. Baum. 1986. Parental influences and smolt size and sex ratio effects on sea age at first maturity of Atlantic salmon (Salmo salar). Can. Spec. Pub. Fish. Aquat. Sci. 89:30-38.
75. Roff, D. 1996. The evolution of threshold traits in animals. Q. Rev. Biol. 71:3-35.
76. Rossiter, M. C. 1996. Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Syst. 27:451-476.
77. Ryan, M. J., C. M. Pease, and M. R. Morris. 1992. A genetic polymorphism in the swordtail Xiphophorus nigrensis: testing the prediction of equal fitnesses. Am. Nat. 139:21-31.
78. Sato, H. 1998. Payoffs of the two alternative nesting tactics in the African dung beetle, Scarabaeus catenatus. Ecol. Entomol. 23:62-67.
79. Simons, A. M., and D. A. Roff. 1994. The effect of environmental variability on the heritabilities of traits of field cricket. Evolution 48:1637-1649.
80. Sinervo, B., and K. R. Zamudio. 2001. The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes. J. Hered. 92:198-205.
81. Slettan, A., I. Olsaker, and Ø. Lie. 1995. Atlantic salmon, Salmo salar, microsatellites at the SSOSL25, SSOSL85, SSOSL311, SSOSL417 loci. Anim. Genet. 26:281-282.
82. Sokal, R. R., and F. J. Rohlf. 1995. Biometry. 3rd ed. W. H. Freeman, San Francisco, CA.
83. StatSoft. 1999. Statistica for Windows. Computer program manual. StatSoft, Inc., Tulsa, OK.
84. Taggart, J. B., I. S. Mclaren, D. W. Hay, J. H. Webb, and A. F. Youngson. 2001. Spawning success in Atlantic salmon (Salmo salar L.): a long-term DNA profiling-based study conducted in a natural stream. Mol. Ecol. 10:1047-1060.
85. Thorpe, J. E., R. I. G. Morgan, C. Talbot, and M. S. Miles. 1983. Inheritance of developmental rate in Atlantic salmon, Salmo salar L. Aquaculture 33:119-128.
86. Weatherhead, P. J., and P. T. Boag. 1997. Genetic estimates of annual and lifetime reproductive success in male red-winged blackbirds. Ecology 78:884-896.
87. Webb, J. H., R. J. Fryer, J. B. Taggart, C. E. Thompson, and A. F. Youngson. 2001. Dispersion of Atlantic salmon (Salmo salar) fry from competing families as revealed by DNA profiling. Can. J. Fish. Aquat. Sci. 58:2386-2395.
88. Whalen, K. G., and D. L. Parrish. 1999. Effect of maturation on parr growth and smolt recruitment of Atlantic salmon. Can. J. Fish. Aquat. Sci. 56:79-86.
89. Wiegmann, D. D., J. R. Baylis, and M. H. Hoff. 1997. Male fitness, body size and timing of reproduction in smallmouth bass, Micropterus dolomieui. Ecology 78:111-128.
90. Wolf, J. B., and M. J. Wade. 2001. On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol. 14:347-356.
91. Zamudio, K. R., and B. Sinervo. 2000. Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proc. Natl Acad. Sci. USA 97:14427-14432.