Abstract
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.
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References
Beacham TD, Murray CB (1993) Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus). J Fish Biol 42:485–508
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 120:1413–1419
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 122:550–559
Braun DC, Patterson DA, Reynolds JD (2013) Maternal and environmental influences on egg size and juvenile life-history traits in Pacific salmon. Ecol Evol 3:1727–1740
Campbell B, Beckman BR, Fairgrieve WT, Dickey JT, Swanson P (2006) Reproductive investment and growth history in female coho salmon. Trans Amer Fish Soc 135:164–173
Crawford SS, Muir AM (2008) Global introductions of salmon and trout in the genus Oncorhynchus: 1870–2007. Revs Fish Biol Fish 18:313–344
Crozier LG, Hutchings JA (2014) Plastic and evolutionary responses to climate change in fish. Evol Appl 7:68–87
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 102:334–345
Donaldson LR, Menasveta D (1961) Selective breeding of chinook salmon. Trans Amer Fish Soc 90:160–164
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: 1–12
Einum S, Hendry AP, Fleming IA (2002) Egg-size evolution in aquatic environments: does oxygen availability constrain size? Proc Royal Soc Lond (Ser B) 269:2325–2330
Elgar MA (1990) Evolutionary compromise between a few large and many small eggs: comparative evidence in teleost fish. Oikos 59:283–287
Fleming IA, Gross MR (1990) Latitudinal clines: a trade-off between egg number and size in Pacific salmon. Ecology 71:1–11
Fleming IA, Ng S (1987) Evaluation of techniques for fixing, preserving, and measuring salmon eggs. Can J Fish Aquat Sci 44:1957–1962
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 264–294
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 106:404–420
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 82:173–211
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 68:1590–1602
Graynoth E (1995) Spawning migrations and reproduction of landlocked sockeye salmon (Oncorhynchus nerka) in the Waitaki catchment, New Zealand. NZ J Mar Freshw Res 29:257–269
Green SJ, Côté IM (2014) Trait-based diet selection: prey behaviour and morphology predict vulnerability to predation in reef fish communities. J Anim Ecol 83:1451–1460
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 144:2733–2738
Haas TC, Blum MJ, Heins DC (2010) Morphological responses of a stream fish to water impoundment. Biol Lett 6:803–806
Healey MC (2001) Patterns of gametic investment by female stream- and ocean-type chinook salmon. J Fish Biol 58:1545–1556
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, USA
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 3:5031–5044
Hutchings JA (2011) Old wine in new bottles: reaction norms in salmonid fishes. Heredity 106:421–437
Hutchings JA (2014) Unintentional selection, unanticipated insights: introductions, stocking, and the evolutionary ecology of fishes. J Fish Biol 85:1907–1926
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 24:25–37
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 46:157–174
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 49:1–9
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 55:1656–1667
MacCrimmon HR, Campbell JS (1969) World distribution of brook trout, Salvelinus fontinalis. J Fish Res Board Can 26:1699–1725
MacCrimmon HR, Marshall TL, Gots BL (1970) World distribution of brown trout, Salmo trutta: further observations. J Fish Res Board Can 27:811–818
McGurk MD (2000) Comparison of fecundity-length-latitude relationships between nonanadromous (kokanee) and anadromous sockeye salmon (Oncorhynchus nerka). Can J Zool 78:1791–1805
Meisner JD, Rosenfeld JS, Regier HA (1988) The role of groundwater in the impact of climate warming on stream salmonines. Fisheries 13(3):2–8
Merilä J, Hendry AP (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol Appl 7:1–14
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 56:1585–1589
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 74:699–705
Murray CB, McPhail JD, Rosenau ML (1989) Reproductive and developmental biology of kokanee from Upper Arrow Lake, British Columbia. Trans Amer Fish Soc 118:503–509
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 67:1–4
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: 72–90
Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle
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 74:425–438
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 127:517–534
Quinn TP, Kinnison MT, Unwin MJ (2001) Evolution of chinook salmon (Oncorhynchus tshawytscha) populations in New Zealand: pattern, rate, and process. Genetica 112(113):493–513
R Development Core Team (2011) R: a language and environment for statistical computing. In: R foundation for Statistical Computing, Vienna, Austria
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 19–160
Rombough PJ (2007) Oxygen as a constraining factor in egg size evolution in salmonids. Can J Fish Aquat Sci 64:692–699
Rounsefell GA (1957) Fecundity of North American Salmonidae. Fish Bull 57:451–468
Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Amer Nat 108:499–506
Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207
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 50:401–416
Vernon EH (1957) Morphometric comparison of three races of kokanee (Oncorhynchus nerka) within a large British Columbia lake. J Fish Res Board Can 14:573–598
Waples RS (1995) Evolutionarily significant units and the conservation of biological diversity under the Endangered Species Act. Amer Fish Soc Symp 17:8–27
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 59:1–41
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 23:559–568
Westley PAH (2011) What invasive species reveal about the rate and form of contemporary phenotypic change in nature. Amer Nat 177:496–509
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 82:128–141
Winemiller KO, Rose KA (1992) Patterns of life-history diversification in North American fishes: implications for population regulation. Can J Fish Aquat Sci 49:2196–2218
Winemiller KO, Rose KA (1993) Why do most fish produce so many tiny offspring? Amer Nat 142:585–603
Winter BD, Crain P (2008) Making the case for ecosystem restoration by dam removal in the Elwha River, Washington. Northwest Sci 82: 13–28
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 47:2250–2260
Wood CC, Foote CJ (1996) Evidence for sympatric genetic divergence of anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 50:1265–1279
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 1–12
Acknowledgments
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.
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Quinn, T.P., Bond, M.H. & Berge, H.B. 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. Ecol Res 30, 547–554 (2015). https://doi.org/10.1007/s11284-015-1255-5
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DOI: https://doi.org/10.1007/s11284-015-1255-5