, Volume 112, Issue 1, pp 515–534 | Cite as

Adaptive divergence and the evolution of reproductive isolation in the wild: an empirical demonstration using introduced sockeye salmon

  • Andrew P. Hendry


Populations exposed to different ecological environments should diverge for phenotypic traits that influence survival and reproduction. This adaptive divergence should reduce gene flow between populations because immigrants become less fit than residents and because hybrids perform poorly in either environment (i.e., ecologically-dependent reproductive isolation). Here I demonstrate adaptive divergence and the evolution of reproductive isolation in populations of sockeye salmon (Oncorhynchus nerka) introduced from a common ancestral source into a new lake system (Lake Washington, Washington). The introduced fish founded several new populations, two of which experience very different environments during breeding and early development (Cedar River v.s. Pleasure Point beach). Over 13 generations, the two populations diverged for adult traits (female body size, male body depth; measured in the wild) and embryo traits (survival to hatching, development rate, size at emergence; measured in a common environment). The rates of divergence for these characters were similar to those observed in other examples of ‘rapid evolution’, and can best be attributed to natural selection. Partial reproductive isolation has evolved in concert with adaptive divergence: the rate of exchange of adults between the populations (determined using natural tags) is higher than the rate of gene flow (determined using DNA microsatellites). The demonstration that adaptive divergence can initiate reproductive isolation in less than 13 generations suggests that the first signs of ‘ecological speciation’ may appear soon after new environments are first colonized.

adaptation adaptive divergence adaptive radiation ecological speciation evolutionary rate microevolution natural selection reproductive isolation sockeye salmon 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anderson, E.C., 1997. Inferring the ancestral origin of sockeye salmon, Oncorhynchus nerka, in the Lake Washington basin: a statistical method in theory and application. Master' Thesis, University of Washington, Seattle.Google Scholar
  2. Beacham, T.D. & C.B. Murray, 1989. Variation in developmental biology of sockeye salmon (Oncorhynchus nerka) and chinook salmon (O. tshawytscha) in British Columbia. Can. J. Zool. 67: 2081–2089.Google Scholar
  3. Blair, G.R., D.E. Rogers & T.P. Quinn, 1993. Variation in life history characteristics and morphology of sockeye salmon in the Kvichak River system, Bristol Bay, Alaska. Trans. Am. Fish. Soc. 122: 550–559.Google Scholar
  4. Brannon, E.L., 1987. Mechanisms stabilizing salmonid fry emergence timing. Can. Spec. Publ. Fish. Aquat. Sci. 96: 120–124.Google Scholar
  5. Burger, C.V., K.T. Scribner, W.J. Spearman, C.O. Swanton & D.E. Campton, 2000. Genetic contribution of three introduced life history forms of sockeye salmon to colonization of Frazer Lake, Alaska. Can. J. Fish. Aquat. Sci. 57: 2096–2111.Google Scholar
  6. Burgner, R.L., 1991. Sockeye salmon, pp. 3–117 in Pacific Salmon Life Histories, edited by C. Groot & L. Margolis. UBC Press, Vancouver, B.C.Google Scholar
  7. Carroll, S.P., H. Dingle, T.R. Famula & C.W. Fox, 2001. Genetic architecture of adaptive differentiation in evolving host races of the soapberry bug, Jadera haematoloma. Genetica 112-113: 257–272.Google Scholar
  8. Cooper, V.S. & R.E. Lenski, 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.Google Scholar
  9. Dobzhansky, T., 1951. Genetics and the Origin of Species. Columbia University Press, New York, N.Y., 3rd edn.Google Scholar
  10. Einum, S. & I.A. Fleming, 2000a. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54: 628–639.Google Scholar
  11. Einum, S. & I.A. Fleming, 2000b. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405: 565–567.Google Scholar
  12. Endler, J.A., 1980. Natural selection on color patterns in Poecilia reticulata. Evolution 34: 76–91.Google Scholar
  13. Endler, J.A., 1986. Natural Selection in the Wild. Princeton University Press, Princeton.Google Scholar
  14. Feder, J.L., S.B. Opp, B. Wlazlo, K. Reynolds, W. Go & S. Spisak, 1994. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 91: 7990–7994.Google Scholar
  15. Filchak, K.E., J.B. Roethele & J.L. Feder, 2000. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407: 739–742.Google Scholar
  16. Fleming, I.A. & M.R. Gross, 1994. Breeding competition in a Pacific salmon (coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 48: 637–657.Google Scholar
  17. Foote, C.J., 1990. An experimental comparison of male and female spawning territoriality in a Pacific salmon. Behaviour 115: 283–314.Google Scholar
  18. Gilchrist, G.W., R.B. Huey & L. Serra, 2001. Rapid evolution of wing size clines in Drosophila subobscura. Genetica 112-113: 273–286.Google Scholar
  19. Gustafson, R.G., R. Waples, S.T. Kalinowski & G.A. Winans, 2001. Evolution of sockeye salmon ecotypes. Science 291: 251.Google Scholar
  20. Gustafson, R.G., T.C. Wainwright, G.A. Winans, F.W. Waknitz, L.T. Parker & R.S. Waples, 1997. Status review of sockeye salmon from Washington and Oregon. U.S. Department of Commerce, NOAA Technical Memorandum, NMFS-NWFSC-33 (available at Scholar
  21. Haldane, J.B.S., 1949. Suggestions as to quantitative measurement of rates of evolution. Evolution 3: 51–56.Google Scholar
  22. Hamon, T.R., C.J. Foote, R. Hilborn & D.E. Rogers, 2000. Selection on morphology of spawning wild sockeye salmon by a gill-net fishery. Trans. Am. Fish. Soc. 129: 1300–1315.Google Scholar
  23. Haugen, T.O., 2000a. Early survival and growth in populations of grayling with recent common ancestors - field experiments. J. Fish Biol. 56: 1173–1191.Google Scholar
  24. Haugen, T.O., 2000b. Growth and survival effects on maturation pattern in populations of grayling with recent common ancestors. Oikos 90: 107–118.Google Scholar
  25. Haugen, T.O., 2000c. Life-history evolution in grayling: evidence for adaptive phenotypic divergence during 8-28 generations. PhD Thesis, University of Oslo, Norway.Google Scholar
  26. Haugen, T.O. & L.A. Vøllestad, 2000. Population differences in early life-history traits in grayling. J. Evol. Biol. 13: 897–905.Google Scholar
  27. Haugen, T.O. & L.A. Vøllestad, 2001. A century of life-history evolution in grayling. Genetica 112-113: 475–491.Google Scholar
  28. Hauser, L., G.R. Carvalho & T.J. Pitcher, 1995. Morphological and genetic differentiation of the African clupeid Limnothrissa miodon 34 years after its introduction into Lake Kivu. J. Fish Biol. 47(suppl. A): 127–144.Google Scholar
  29. Healey, M.C., 1987. The adaptive significance of age and size at maturity in female sockeye salmon (Oncorhynchus nerka). Can. Spec. Publ. Fish. Aquat. Sci. 96: 110–117.Google Scholar
  30. Hendry, A.P., O.K. Berg & T.P. Quinn, 1999. Condition dependence and adaptation-by-time: breeding date, life history, and energy allocation within a population of salmon. Oikos 85: 499–514.Google Scholar
  31. Hendry, A.P., T. Day & E.B. Taylor, 2001. Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution 55: 459–466.Google Scholar
  32. Hendry, A.P., J.E. Hensleigh & R.R. Reisenbichler, 1998. Incubation temperature, developmental biology, and the divergence of sockeye salmon (Oncorhynchus nerka) within LakeWashington. Can. J. Fish. Aquat. Sci. 55: 1387–1394.Google Scholar
  33. Hendry, A.P. & M.T. Kinnison, 1999. The pace of modern life: measuring rates of contemporary microevolution. Evolution 53: 1637–1653.Google Scholar
  34. Hendry, A.P. & T.P. Quinn, 1997. Variation in adult life history and morphology among Lake Washington sockeye salmon (Oncorhynchus nerka) populations in relation to habitat features and ancestral affinities. Can. J. Fish. Aquat. Sci. 54: 75–84.Google Scholar
  35. Hendry, A.P., T.P. Quinn & F.M. Utter, 1996. Genetic evidence for the persistence and divergence of native and introduced sockeye salmon (Oncorhynchus nerka) within LakeWashington, Washington. Can. J. Fish. Aquat. Sci. 53: 823–832.Google Scholar
  36. Hendry, A.P., J.K. Wenburg, P. Bentzen, E. Volk & T.P. Quinn, 2000. Rapid evolution of reproductive isolation in the wild: evidence from introduced salmon. Science 290: 516–518.Google Scholar
  37. Hendry, A.P., J.K. Wenburg, P. Bentzen, E. Volk & T.P. Quinn, 2001a. Evolution of sockeye salmon ecotypes - response. Science 291: 251–252.Google Scholar
  38. Hendry, A.P., J.K. Wenburg, P. Bentzen, E. Volk & T.P. Quinn, 2001b. Examining evidence of reproductive isolation in sockeye salmon - response. Science 291: 1853a.Google Scholar
  39. Higgie, M., S. Chenoweth & M.W. Blows, 2000. Natural selection and the reinforcement of mate recognition. Science 290: 519–521.Google Scholar
  40. Hill, J.K., C.D. Thomas & D.S. Blakeley, 1999. Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia 121: 165–170.Google Scholar
  41. Howard, D.J., J.L. Marshall, W.E. Braswell & J.A. Coyne, 2001. Examining evidence of reproductive isolation in sockeye salmon. Science 291: 1853aGoogle Scholar
  42. Kingsolver, J.G., H.E. Hoekstra, J.M. Hoekstra, D. Berrigan, S.N. Vignieri, C.E. Hill, A. Hoang, P. Gibert & P. Beerli, 2001. The strength of phenotypic selection in natural popualations. Am. Nat. 157: 245–261.Google Scholar
  43. Kinnison, M.T. & A.P. Hendry, 2001. The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112-113: 145–164.Google Scholar
  44. Kinnison, M., M. Unwin, N. Boustead & T. Quinn, 1998a. Population-specific variation in body dimensions of adult chinook salmon (Oncorhynchus tshawytscha) from New Zealand and their source population, 90 years after introduction. Can. J. Fish. Aquat. Sci. 55: 554–563.Google Scholar
  45. Kinnison, M.T., M.J. Unwin, W.K. Hershberger & T.P. Quinn, 1998b. Egg size, fecundity, and development rate of two introduced New Zealand chinook salmon (Oncorhynchus tshawytscha) populations. Can. J. Fish. Aquat. Sci. 55: 1946–1953.Google Scholar
  46. Kinnison, M.T., M.J. Unwin & T.P. Quinn, 1998. Growth and salinity tolerance of juvenile chinook salmon (Oncorhynchus tshawytscha) from two introduced New Zealand populations. Can. J. Zool. 76: 2219–2226.Google Scholar
  47. Klepaker, T., 1993. Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can. J. Zool. 71: 1251–1258.Google Scholar
  48. Lande, R., 1976. Natural selection and random genetic drift in phenotypic evolution. Evolution 30: 314–334.Google Scholar
  49. Lande, R., 1977. Statistical tests for natural selection on quantitative characters. Evolution 31: 442–444.Google Scholar
  50. Lande, R. & M. Kirkpatrick, 1988. Ecological speciation by sexual selection. J. Theor. Biol. 133: 85–98.Google Scholar
  51. Lenski, R.E. & M. Travisano, 1994. Dynamics of adaptation and diversification: a 10,000–generation experiment with bacterial populations. Proc. Natl. Acad. Sci. USA 91: 6808–6814.Google Scholar
  52. Liou, L.W. & T.D. Price, 1994. Speciation by reinforcement of premating isolation. Evolution 48: 1451–1459.Google Scholar
  53. Losos, J.B., K.I. Warheit & T.W. Schoener, 1997. Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387: 70–73.Google Scholar
  54. Losos, J.B., T.W. Schoener, K.I. Warheit & D. Creer, 2001. Experimental studies of adaptive divergence in Bahamian Anolis lizards. Genetica 112-113: 399–415.Google Scholar
  55. Lu, G. & L. Bernatchez, 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution 53: 1491–1505.Google Scholar
  56. Magurran, A.E., B.H. Seghers, P.W. Shaw & G.R. Carvalho, 1995. The behavioral diversity and evolution of guppy, Poecilia reticulata, populations in Trinidad. Adv. Study Behav. 24: 155–202.Google Scholar
  57. Mayr, E., 1942. Systematics and the Origin of Species. Columbia University Press, New York, N.Y.Google Scholar
  58. Montgomery, D.R., J.M. Buffington, N.P. Peterson, D. Schuett-Hames & T.P. Quinn, 1996. Stream-bed scour, egg burial depths, and the influence of salmonid spawning on bed surface mobility and embryo survival. Can. J. Fish. Aquat. Sci. 53: 1061–1070.Google Scholar
  59. Moore, K., 1996. The adaptive significance of body size and shape in sexually mature sockeye salmon Oncorhynchus nerka. Master' Thesis, University of Washington, Seattle.Google Scholar
  60. Nagel, L. & D. Schluter, 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52: 209–218.Google Scholar
  61. Quinn, T.P. & C.J. Foote, 1994. The effects of body size and sexual dimorphism on the reproductive behaviour of sockeye salmon, Oncorhynchus nerka. Anim. Behav. 48: 751–761.Google Scholar
  62. Quinn, T.P., A.P. Hendry & L.A. Wetzel, 1995. The influence of life history trade-offs and the size of incubation gravels on egg size variation in sockeye salmon (Oncorhynchus nerka). Oikos 74: 425–438.Google Scholar
  63. Quinn, T.P., M.D. Adkison & M.B. Ward, 1996. Behavioral tactics of male sockeye salmon (Oncorhynchus nerka) under varying operational sex ratios. Ethology 102: 304–322.Google Scholar
  64. Quinn, T.P., E.C. Volk & A.P. Hendry, 1999. Natural otolith microstructure patterns reveal precise homing to natal incubation sites by sockeye salmon (Oncorhynchus nerka). Can. J. Zool. 77: 766–775.Google Scholar
  65. Quinn, T.P., M.J. Unwin & M.T. Kinnison, 2000. Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced chinook salmon populations. Evolution 54: 1372–1385.Google Scholar
  66. Quinn, T.P., A.P. Hendry & G.B. Buck, 2001. Balancing natural and sexual selection in sockeye salmon: interactions between body size, reproductive opportunity and vulnerability to predation by bears. Evol. Ecol. Res. (in press).Google Scholar
  67. Quinn, T.P., M.T. Kinnison & M.J. Unwin, 2001. Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern, rate, and process. Genetica 112-113: 493–513.Google Scholar
  68. Reznick, D.N. & H. Bryga, 1987. Life-history evolution in guppies (Poecilia reticulata): 1. phenotypic and genetic changes in an introduction experiment. Evolution 41: 1370–1385.Google Scholar
  69. Reznick, D.N., H. Bryga & J.A. Endler, 1990. Experimentally induced life-history evolution in a natural population. Nature 346: 357–359.Google Scholar
  70. Reznick, D.N., F.H. Shaw, F.H. Rodd & R.G. Shaw, 1997. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275: 1934–1937.Google Scholar
  71. Reznick, D.N. & C.K. Ghalambor, 2001. The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112- 113: 183–198.Google Scholar
  72. Rice, W.R. & E.E. Hostert, 1993. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47: 1637–1653.Google Scholar
  73. Royal, L.A. & A. Seymour, 1940. Building new salmon runs. Prog. Fish-Cult. 52: 1–7.Google Scholar
  74. Ruggerone, G.T., R. Hanson & D.E. Rogers, 2000. Selective predation by brown bears (Ursus arctos) foraging on spawning sockeye salmon (Oncorhynchus nerka). Can. J. Zool. 78: 974–981.Google Scholar
  75. Rundle, H.D., L. Nagel, J.W. Boughman & D. Schluter, 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308.Google Scholar
  76. Rundle, H.D. & M.C. Whitlock, 2001. A genetic interpretation of ecologically dependent isolation. Evolution 55: 198–201.Google Scholar
  77. Schluter, D., 1996a. Ecological causes of adaptive radiation. Am. Nat. 148: S40–S64.Google Scholar
  78. Schluter, D., 1996b. Ecological speciation in postglacial fishes. Phil. Trans. R. Soc. Lond. B. 351: 807–814.Google Scholar
  79. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  80. Shaklee, J.B., J. Ames & L. LaVoy, 1996. Genetic diversity units and major ancestral lineages for sockeye salmon in Washington. Technical Report 95–02/96. Washington Department of Fish and Wildlife, Olympia, W.A.Google Scholar
  81. Seeb, J. & L. Wishard, 1977. The use of biochemical genetics in the management of Pacific salmon stocks: genetic marking and mixed fishery analysis. Final Report, Service Contract No. 792. Washington Department of Fisheries, Olympia, W.A.Google Scholar
  82. Smoker, W.W., A.J. Gharrett, M.S. Stekoll & J.E. Joyce, 1994. Genetic analysis of size in an anadromous population of pink salmon. Can. J. Fish. Aquat. Sci. 51(suppl. 1): 9–15.Google Scholar
  83. Steen, R.P. & T.P. Quinn, 1999. Egg burial depth by sockeye salmon (Oncorhynchus nerka): implications for survival of embryos and natural selection on female body size. Can. J. Zool. 77: 836–841.Google Scholar
  84. Tallman, R.F. & M.C. Healey, 1991. Phenotypic differentiation in seasonal ecotypes of chum salmon, Oncorhynchus keta. Can. J. Fish. Aquat. Sci. 48: 661–671.Google Scholar
  85. Taylor, E.B., 1999. Species pairs of north temperate freshwater fishes: evolution, taxonomy, and conservation. Rev. Fish Biol. Fisher. 9: 299–324.Google Scholar
  86. Thorne, R.E. & J.J. Ames, 1987. A note on variability of marine survival of sockeye salmon (Oncorhynchus nerka) and effects of flooding on spawning success. Can. J. Fish. Aquat. Sci. 44: 1791–1795.Google Scholar
  87. Turesson, G., 1922. The genotypic response of the plant species to the habitat. Hereditas 3: 211–350.Google Scholar
  88. Varnavskaya, N.V., C.C. Wood, R.J. Everett, R.L. Wilmot, V.S. Varnavsky, V.V. Midanaya & T.P. Quinn, 1994. Genetic differentiation of subpopulations of sockeye salmon (Oncorhynchus nerka) within lakes of Alaska, British Columbia and Kamchatka, Russia. Can. J. Fish. Aquat. Sci. 51(suppl. 1): 147–157.Google Scholar
  89. Via, S., 1999. Reproductive isolation between sympatric races of pea aphids. I: gene flow restriction and habitat choice. Evolution 53: 1446–1457.Google Scholar
  90. Via, S., A.C. Bouck & S. Skillman, 2000. Reproductive isolation between divergent races of pea aphids on two hosts. II: selection against migrants and hybrids in the parental environments. Evolution 54: 1626–1637.Google Scholar
  91. Wetzel, L., 1993. Genetic, morphometric and life history characteristics of sockeye salmon (Oncorhynchus nerka) in the Wood River Lake system, Alaska. Master' Thesis, University of Washington, Seattle.Google Scholar
  92. Winans, G.A., P.B. Aebersold & R.S. Waples, 1996. Allozyme variability of Oncorhynchus nerka in the Pacific Northwest, with special consideration to populations of Redfish Lake, Idaho. Trans. Am. Fish. Soc. 125: 645–663.Google Scholar
  93. Wood, C.C., 1995. Life history variation and population structure in sockeye salmon, pp. 195–216 in Evolution and the Aquatic Ecosystem, edited by J.L. Nielsen. American Fisheries Society Symposium 17, Bethesda, M.D.Google Scholar
  94. Woodey, J.C., 1966. Sockeye salmon spawning grounds and adult returns in the Lake Washington watershed, 1965. Master' Thesis, University of Washington, Seattle.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Andrew P. Hendry
    • 1
  1. 1.Organismic and Evolutionary Biology ProgramUniversity of MassachusettsAmherstUSA

Personalised recommendations