Ecological Research

, Volume 30, Issue 3, pp 547–554 | Cite as

Use of egg size differences in anadromous (sockeye salmon) and non-anadromous (kokanee) forms of Oncorhynchus nerka to infer ancestral origins of a landlocked population

  • Thomas P. Quinn
  • Morgan H. Bond
  • Hans B. Berge
Original Article


Life history traits reflect interactions between evolutionary lineage and environmental conditions. Translocations of populations to new environments, and changes in their natal environment, provide insights into the factors controlling life history. For example, the trade-off between egg size and egg number is a well-studied adaptation in fishes, and especially salmon and trout. We used existing and new data on this tradeoff in anadromous sockeye salmon, Oncorhynchus nerka, and the non-anadromous form of the species (kokanee), to investigate the likely origin of a population of uncertain ancestry, land-locked for a century above an impassable dam. Native kokanee have smaller eggs than do the larger-bodied anadromous sockeye salmon. However, the land-locked population in Lake Sutherland, in the Elwha River system, Washington, USA had much larger eggs for their body size than any other kokanee population, similar only to the land-locked descendants of anadromous sockeye salmon in New Zealand. After evaluating and rejecting a series of competing explanations for the unusually large eggs, we infer that the population was mostly likely of anadromous origin, retaining the ancestral tendency to produce large eggs, despite the sacrifice in fecundity that is necessitated by the limited female energy resources. This study revealed the utility of life history traits for studying the ancestral origins of a population for which molecular genetic tools were not informative. Worldwide, many populations have been transplanted or exposed to new conditions, affording similar opportunities to investigate phenotypic plasticity and evolutionary adaptations.


Life history Trade-offs Fecundity Salmonid fishes 



We thank Marcia House (Northwest Indian Fish Commission) and Michael McHenry (Lower Elwha Klallam Tribe) for providing us with access to fish caught in Lake Sutherland, Daniel Hasselman, Jon Wittouck, Emily Thornton, Daniel Lantz, and Jim Lissa for help processing the samples, Nicola Follis for measuring photographed fish, and Darin Combs, John Kugen, and Larry Sisson (Washington Dept. of Fish and Wildlife) for providing us with access to Lake Sammamish and Lake Whatcom kokanee. We also gratefully acknowledge funding for this study from the Washington Sea Grant program, University of Washington, pursuant to NOAA Award No. NA10OAR4170075, Project R/LME-7, and from the H. Mason Keeler Endowment at the University of Washington, and helpful comments from the reviewers.


  1. Beacham TD, Murray CB (1993) Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus). J Fish Biol 42:485–508CrossRefGoogle Scholar
  2. Beaton LL, Van Zandt PA, Esselman EJ, Knight TM (2011) Comparison of the herbivore defense and competitive ability of ancestral and modern genotypes of an invasive plant, Lespedeza cuneate. Oikos 120:1413–1419CrossRefGoogle Scholar
  3. Blair GR, Rogers DE, Quinn TP (1993) Variation in life history characteristics and morphology of sockeye salmon in the Kvichak River system, Bristol Bay, Alaska. Trans Amer Fish Soc 122:550–559CrossRefGoogle Scholar
  4. Braun DC, Patterson DA, Reynolds JD (2013) Maternal and environmental influences on egg size and juvenile life-history traits in Pacific salmon. Ecol Evol 3:1727–1740CrossRefPubMedCentralPubMedGoogle Scholar
  5. Campbell B, Beckman BR, Fairgrieve WT, Dickey JT, Swanson P (2006) Reproductive investment and growth history in female coho salmon. Trans Amer Fish Soc 135:164–173CrossRefGoogle Scholar
  6. Crawford SS, Muir AM (2008) Global introductions of salmon and trout in the genus Oncorhynchus: 1870–2007. Revs Fish Biol Fish 18:313–344CrossRefGoogle Scholar
  7. Crozier LG, Hutchings JA (2014) Plastic and evolutionary responses to climate change in fish. Evol Appl 7:68–87CrossRefPubMedCentralPubMedGoogle Scholar
  8. Diamantidis AD, Carey JR, Nakas CT, Papadopoulos NT (2011) Ancestral populations perform better in a novel environment: domestication of medfly populations from five global regions. Biol J Linn Soc Lond 102:334–345CrossRefPubMedCentralPubMedGoogle Scholar
  9. Donaldson LR, Menasveta D (1961) Selective breeding of chinook salmon. Trans Amer Fish Soc 90:160–164CrossRefGoogle Scholar
  10. Duda JJ, Freilich JE, Schreiner EG (2008) Baseline studies in the Elwha River ecosystem prior to dam removal: introduction to the special issue. Northwest Sci 82: 1–12Google Scholar
  11. Einum S, Hendry AP, Fleming IA (2002) Egg-size evolution in aquatic environments: does oxygen availability constrain size? Proc Royal Soc Lond (Ser B) 269:2325–2330CrossRefGoogle Scholar
  12. Elgar MA (1990) Evolutionary compromise between a few large and many small eggs: comparative evidence in teleost fish. Oikos 59:283–287CrossRefGoogle Scholar
  13. Fleming IA, Gross MR (1990) Latitudinal clines: a trade-off between egg number and size in Pacific salmon. Ecology 71:1–11CrossRefGoogle Scholar
  14. Fleming IA, Ng S (1987) Evaluation of techniques for fixing, preserving, and measuring salmon eggs. Can J Fish Aquat Sci 44:1957–1962CrossRefGoogle Scholar
  15. Fleming IA, Reynolds JD (2004) Salmonid breeding systems. In: Hendry AP, Stearns SC (eds) Evolution illuminated: Salmon and their relatives. Oxford University Press, Oxford, pp 264–294Google Scholar
  16. Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404–420CrossRefPubMedCentralPubMedGoogle Scholar
  17. Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S, Aubin-Horth N, Lajus D, Letcher BH, Youngson AF, Webb JH, Vøllestad LA, Villanueva B, Ferguson A, Quinn TP (2007) A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Revs 82:173–211CrossRefGoogle Scholar
  18. Godbout L, Wood CC, Withler RE, Latham S, Nelson RJ, Wetzel L, Barnett-Johnson R, Grove MJ, Schmitt AK, McKeegan KD (2011) Sockeye salmon (Oncorhynchus nerka) return after an absence of nearly 90 years: a case of reversion to anadromy. Can J Fish Aquat Sci 68:1590–1602CrossRefGoogle Scholar
  19. Graynoth E (1995) Spawning migrations and reproduction of landlocked sockeye salmon (Oncorhynchus nerka) in the Waitaki catchment, New Zealand. NZ J Mar Freshw Res 29:257–269CrossRefGoogle Scholar
  20. Green SJ, Côté IM (2014) Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities. J Anim Ecol 83:1451–1460CrossRefGoogle Scholar
  21. Griffiths AM, Ellis JS, Clifton-Dey D, Machado-Schiaffino G, Bright D, Garcia-Vazquez E, Stevens JR (2011) Restoration versus recolonisation: the origin of Atlantic salmon (Salmo salar L.) currently in the River Thames. Biol Cons 144:2733–2738CrossRefGoogle Scholar
  22. Haas TC, Blum MJ, Heins DC (2010) Morphological responses of a stream fish to water impoundment. Biol Lett 6:803–806CrossRefPubMedCentralPubMedGoogle Scholar
  23. Healey MC (2001) Patterns of gametic investment by female stream- and ocean-type chinook salmon. J Fish Biol 58:1545–1556Google Scholar
  24. Hiss JM, Wunderlich RC (1994) Status of kokanee salmon (Oncorhynchus nerka) in the Lake Sutherland basin and prospects for sockeye salmon restoration. US Fish and Wildlife Service, USAGoogle Scholar
  25. Howeth JG, Weis JJ, Brodersen J, Hatton EC, Post DM (2013) Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure. Ecol Evol 3:5031–5044CrossRefPubMedCentralPubMedGoogle Scholar
  26. Hutchings JA (2011) Old wine in new bottles: reaction norms in salmonid fishes. Heredity 106:421–437CrossRefPubMedCentralPubMedGoogle Scholar
  27. Hutchings JA (2014) Unintentional selection, unanticipated insights: introductions, stocking, and the evolutionary ecology of fishes. J Fish Biol 85:1907–1926CrossRefPubMedGoogle Scholar
  28. Ibáñez I, Diez JM, Miller LP, Olden JD, Sorte CJB, Blumenthal DM, Bradley BA, D’Antonio CM, Dukes JS, Early RI, Grosholz ED, Lawler JJ (2014) Integrated assessment of biological invasions. Ecol Appl 24:25–37CrossRefPubMedGoogle Scholar
  29. Kaeriyama M, Urawa S, Suzuki T (1992) Anadromous sockeye salmon (Oncorhynchus nerka) derived from nonanadromous kokanees: life history in Lake Toro. Sci Repts Hokkaido Salmon Hatchery 46:157–174Google Scholar
  30. Kaeriyama M, Urawa S, Fukuwaka MA (1995) Variation in body size, fecundity, and egg size of sockeye and kokanee salmon, Oncorhynchus nerka, released from hatchery. Sci Repts Hokkaido Salmon Hatchery 49:1–9Google Scholar
  31. Kinnison MT, Unwin MJ, Hendry AP, Quinn TP (2001) Migratory costs and the evolution of egg size and number allocation in new and indigenous salmon populations. Evolution 55:1656–1667CrossRefPubMedGoogle Scholar
  32. MacCrimmon HR, Campbell JS (1969) World distribution of brook trout, Salvelinus fontinalis. J Fish Res Board Can 26:1699–1725CrossRefGoogle Scholar
  33. MacCrimmon HR, Marshall TL, Gots BL (1970) World distribution of brown trout, Salmo trutta: further observations. J Fish Res Board Can 27:811–818CrossRefGoogle Scholar
  34. McGurk MD (2000) Comparison of fecundity-length-latitude relationships between nonanadromous (kokanee) and anadromous sockeye salmon (Oncorhynchus nerka). Can J Zool 78:1791–1805CrossRefGoogle Scholar
  35. Meisner JD, Rosenfeld JS, Regier HA (1988) The role of groundwater in the impact of climate warming on stream salmonines. Fisheries 13(3):2–8CrossRefGoogle Scholar
  36. Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14CrossRefPubMedCentralPubMedGoogle Scholar
  37. Morita K, Yamamoto S, Takashima Y, Matsuishi T, Kanno Y, Nishimura K (1999) Effect of maternal growth history on egg number and size in wild white-spotted char (Salvelinus leucomaenis). Can J Fish Aquat Sci 56:1585–1589CrossRefGoogle Scholar
  38. Morita K, Tamate T, Sugimoto Y, Tago Y, Watanabe T, Konaka H, Sato M, Miyauchi Y, Ohkuma K, Nagasawa T (2009) Latitudinal variation in egg size and number in anadromous masu salmon Oncorhynchus masou. J Fish Biol 74:699–705CrossRefPubMedGoogle Scholar
  39. Murray CB, McPhail JD, Rosenau ML (1989) Reproductive and developmental biology of kokanee from Upper Arrow Lake, British Columbia. Trans Amer Fish Soc 118:503–509CrossRefGoogle Scholar
  40. Perrier C, Evanno G, Belliard J, Guyomard R, Baglinière J-L (2010) Natural recolonization of the Seine River by Atlantic salmon (Salmo salar) of multiple origins. Can J Fish Aquat Sci 67:1–4CrossRefGoogle Scholar
  41. Pess GR, McHenry ML, Beechie TJ, Davies J (2008) Biological impacts of the Elwha River dams and potential salmonid responses to dam removal. Northwest Sci 82: 72–90Google Scholar
  42. Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University of Washington Press, SeattleGoogle Scholar
  43. Quinn TP, Hendry AP, Wetzel LA (1995) The influence of life history trade-offs and the size of incubation gravels on egg size variation in sockeye salmon (Oncorhynchus nerka). Oikos 74:425–438CrossRefGoogle Scholar
  44. Quinn TP, Graynoth E, Wood CC, Foote CJ (1998) Genotypic and phenotypic divergence of sockeye salmon in New Zealand from their ancestral British Columbia populations. Trans Amer Fish Soc 127:517–534CrossRefGoogle Scholar
  45. Quinn TP, Kinnison MT, Unwin MJ (2001) Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern, rate, and process. Genetica 112(113):493–513CrossRefPubMedGoogle Scholar
  46. R Development Core Team (2011) R: a language and environment for statistical computing. In: R foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  47. Ricker WE (1972) Hereditary and environmental factors affecting certain salmonid populations. In: Simon RC, Larkin PA (eds) The stock concept in Pacific salmon. MacMillan Lectures in Fisheries, University of British Columbia Press, Vancouver, Columbia, pp 19–160Google Scholar
  48. Rombough PJ (2007) Oxygen as a constraining factor in egg size evolution in salmonids. Can J Fish Aquat Sci 64:692–699CrossRefGoogle Scholar
  49. Rounsefell GA (1957) Fecundity of North American Salmonidae. Fish Bull 57:451–468Google Scholar
  50. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Amer Nat 108:499–506CrossRefGoogle Scholar
  51. Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207CrossRefGoogle Scholar
  52. Taylor EB, Foote CJ, Wood CC (1996) Molecular genetic evidence for parallel life-history evolution within a Pacific salmon (sockeye salmon and kokanee, Oncorhynchus nerka). Evolution 50:401–416CrossRefGoogle Scholar
  53. Vernon EH (1957) Morphometric comparison of three races of kokanee (Oncorhynchus nerka) within a large British Columbia lake. J Fish Res Board Can 14:573–598CrossRefGoogle Scholar
  54. Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Amer Fish Soc Symp 17:8–27Google Scholar
  55. Waples RS, Gustafson RG, Weitkamp LA, Myers JM, Johnson OW, Busby PJ, Hard JJ, Bryant GJ, Waknitz FW, Neely K, Teel D, Grant WS, Winans GA, Phelps S, Marshall A, Baker BM (2001) Characterizing diversity in salmon from the Pacific Northwest. J Fish Biol 59:1–41Google Scholar
  56. Ward-Fear G, Brown GP, Greenlees MJ, Shine R (2009) Maladaptive traits in invasive species: in Australia, cane toads are more vulnerable to predatory ants than are native frogs. Funct Ecol 23:559–568CrossRefGoogle Scholar
  57. Westley PAH (2011) What invasive species reveal about the rate and form of contemporary phenotypic change in nature. Amer Nat 177:496–509CrossRefGoogle Scholar
  58. Winans GA, McHenry M, Baker J, Elz A, Goodbla A, Iwamoto E, Kuligowski D, Miller KM, Small MP, Spruell P, Van Doornik D (2008) Genetic inventory of anadromous Pacific salmonids of the Elwha River prior to dam removal. Northwest Sci 82:128–141CrossRefGoogle Scholar
  59. Winemiller KO, Rose KA (1992) Patterns of life-history diversification in North American fishes: implications for population regulation. Can J Fish Aquat Sci 49:2196–2218CrossRefGoogle Scholar
  60. Winemiller KO, Rose KA (1993) Why do most fish produce so many tiny offspring? Amer Nat 142:585–603CrossRefGoogle Scholar
  61. Winter BD, Crain P (2008) Making the case for ecosystem restoration by dam removal in the Elwha River, Washington. Northwest Sci 82: 13–28Google Scholar
  62. Wood CC, Foote CJ (1990) Genetic differences in the early development and growth of sympatric sockeye salmon and kokanee (Oncorhynchus nerka), and their hybrids. Can J Fish Aquat Sci 47:2250–2260CrossRefGoogle Scholar
  63. Wood CC, Foote CJ (1996) Evidence for sympatric genetic divergence of anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 50:1265–1279CrossRefGoogle Scholar
  64. Wootton RJ (1984) Introduction: strategies and tactics in fish reproduction. In: Potts GW, Wootton RJ (eds) Fish reproduction—strategies and tactics. Academic Press, London, pp 1–12Google Scholar

Copyright information

© The Ecological Society of Japan 2015

Authors and Affiliations

  • Thomas P. Quinn
    • 1
  • Morgan H. Bond
    • 1
  • Hans B. Berge
    • 2
  1. 1.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA
  2. 2.King County Department of Natural Resources and ParksSeattleUSA

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