Life histories of anadromous salmon males reveal a trade-off between primary and secondary sexual traits

Tomislav Vladić, Torbjörn Järvi, Erik Petersson

Paper category: Original research paper
Corresponding author: Tomislav Vladić (
DOI: 10.2478/ohs-2019-0025
Received: 06/11/2018
Accepted: 12/03/2019
Full text: here

Citation: Vladić, T., Järvi, T. & Petersson, E. (2019). Life histories of anadromous salmon males reveal a trade-off between primary and secondary sexual traits. Oceanological and Hydrobiological Studies, 48(3), pp. 279-289. Retrieved 3 Oct. 2019, from doi:10.2478/ohs-2019-0025


The life-history trade-off between investment in somatic growth and gonadal tissue is caused by individual energy limitations and results in individuals that adopt specific tactics to achieve reproduction. Allocation in primary and secondary sexual traits in Atlantic salmon males was studied by assessing life history traits (smolt size, sea age, growth rate) based on back-calculation of scales, ejaculate energy content (sperm ATP content, mass and density) and the size of secondary sexual traits. We found that males investing less in secondary sexual traits produce ejaculates with a higher energy content. Differences were found in the investment into primary and secondary sexual traits between fish that spent one year in the sea before returning to their spawning grounds (grilse) and multi-sea-winter adults, suggesting that different energy allocation patterns in reproductive effort reflect alternative developmental pathways. These findings are consistent with the pattern where multi-sea-winter male ejaculate investment relies principally on the resource acquisition in the ocean, whereas grilse ejaculate investment relies chiefly on the resource allocation of available surplus energy, thus representing alternative male reproductive tactics.


Aas, G.H. Gjerde, B. & Refstie, T. (1991). Evaluation of milt quality of Atlantic salmon. Aquaculture 95: 125–132. DOI: 10.1016/0044-8486(91)90079-M.
Alm, G. (1959). Connection between maturity, size and age in fishes. Reports from the Institute for Freshwater Research, Drottningholm 40: 5–145.
Andersson, M. & Simmons, L.W. (2006). Sexual selection and mate choice. Trends in Ecology and Evolution 21: 296–302. DOI: 10.1016/j.tree.2006.03.015.
Avise, J.C., Jones, AG, Walker, D. & DeWoody, J.A., collaborators. (2002). Genetic mating systems and reproductive natural histories of fishes: Lessons for ecology and evolution. Annual Reviews in Genetics 36: 19–45. DOI: 10.1146/annurev.genet.36.030602.090831.
Barson, N.J., Aykanat, T., Hindar, K., Baranski, M., Bolstad, G.H. et al. (2015). Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 405: 405–408. DOI: 10.1038/nature16062.
Charnov, E.L. & Berrigan, D. (1991). Evolution of life history parameters in animals with indeterminate growth, particularily fish. Evolutionary Ecology 5: 63–68. DOI: 10.1007/BF02285246.
Christen, R., Gatti, J-L. & Billard, R. (1987). Trout sperm motility. The transient movement of trout sperm is related to changes in the concentration of ATP following the activation of the flagelar movement. European Journal of Biochemistry 160: 667–671. DOI: 10.1111/j.1432-1033.1987.tb13565.x.
Cosson, J., Billard, R., Cibert, C., Dréanno, C & Suquet, M. (1999). Ionic factors regulating the motility of fish sperm. In C. Gagnon (Ed.), The Male Gamete: From Basic Science to Clinical Applications (pp. 161–186). Cache River Press.
Doyle, R.W., Talbot, A.J. & Nicholas, R.R. (1987). Statistical interrelation of length, growth, and scale intercirculi spacing: Appraisal of a growth rate estimator for fish. Canadian Journal of Fisheries and Aquatic Sciences 44: 1520–1528. DOI: 10.1139/f87-183.
Emlen, S.T & Oring, L.V. (1977). Ecology, sexual selection and the evolution of mating systems. Science 197: 215–223.
Evans, J.P. (2010). Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proceedings of the Royal Society London B 277: 3195–3201. DOI: 10.1098/rspb.2010.0826.
Flannery, E.W., Butts, I.A, Slowinska, M., Cierzsko, A. & Pitcher, T.E. (2012). Reproductive investment patterns, sperm characteristics, and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tschawytscha). Biological Journal of the Linnean Society 108: 99–108. DOI: 10.1111/j.1095-8312.2012.01980.x.
Fleming, I.A. (1996). Reproductive strategies of Atlantic salmon: ecology and evolution. Reviews in Fish Biology and Fisheries 6: 379–416. DOI: 10.1007/BF00164323.
Foote, C.J. (1989). Female mate preference in Pacific salmon. Animal Behaviour 38: 721–723. DOI: 10.1016/S0003-3472(89)80022-3.
Gage, M.J.G., Stockley, P. & Parker, G.A. (1995). Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations. Philosophical Transactions of the Royal Society London B 350: 391–399. DOI: 10.1098/rstb.1995.0173.
Garant, D., Dodson, J.J. & Bernatchez, L. (2003). Differential reproductve success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.).Evolution 57: 1133–1141. DOI: 10.1111/j.0014-3820.2003.tb00322.x.
Hampp, R. (1985). Luminometric method. In J. Bergmayer (Ed.), Methods of Enzymatic Analysis 7: 370–379.
Hollo, G. (2015). A new paradigm for animal symmetry. Interface Focus 5(6). DOI: 10.1098/rsfs.2015.0032.
Hutchings, J.A. (2011). Old wine in new bottles: reaction norms in salmonid fishes. Heredity 106: 421–437. DOI: 10.1038/hdy.2010.166.
Järvi, T. (1990). The effects of male dominance, secondary sexual characteristics and female mate choice on the mating success of male Atlantic salmon, Salmo salar. Ethology 84: 123–132. DOI: 10.1111/j.1439-0310.1990.tb00789.x.
de Jong, G. (1995). Phenotypic plasticity as a product of selection in a variable environment. American Naturalist 145: 439–512. DOI: 10.1086/285752.
Jonsson, B. & Jonsson, N. (2005). Lipid energy reserves influence life-history decision of Atlantic salmon (Salmo salar) and brown trout (S. trutta) in fresh water. Ecology of Freshwater Fish 14: 296–301. DOI: 10.1111/j.1600-0633.2005.00098.x.
Jordan W.C., Fleming, I.A. & Garant D. (2007). Mating system and social structure. In E. Verspoor, L. Stradmeyer & J. Nielsen (Eds.), The Atlantic Salmon. Genetics, Conservation and Management (pp. 167–194). Blackwell.
Lehnert, S.J., Helou, L., Pitcher, T.E., Heath, J.W. & Heath, D.D. (2018) Sperm competition, but not major histocompatibility divergence, drive differential fertilization success between alternative reproductive tactics in Chinook salmon. Journal of Evolutionary Biology 31: 88–97. DOI: 10.1111/jeb.13199.
Lindroth, A. (1960). Body/scale relationship in Atlantic salmon. International Council for the Exploration of the Sea 104: 1–25.
Lüpold, S (2013). Ejaculate quality and constraints in relation to sperm competition levels among eutherian mammals. Evolution 67: 3052–3060. DOI: 10.1111/evo.12132.
Michod, R.E. (2007). Evolution of individuality during transition from unicellular to multicellular life. Proceedings of the National Academy of Sciences USA 104: 8613–8616. DOI: 10.1073/pnas.0701489104.
Mjølnerød, I.B., Fleming, I.A., Refseth, U.H. & Hindar, K. (1998). Mate and sperm competition during multiple-male spawning of Atlantic salmon. Canadian Journal of Zoology 76: 70–75. DOI: 10.1139/z97-173.
Neff, B.D., Fu, P. & Gross, M.R. (2003). Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behavioural Ecology 14: 634–641. DOI: 10.1093/beheco/arg032.
van Noordwijk, A.J. & de Jong, G. (1986). Acquisition and allocation of resources: their influence on variation in life history tactics. American Naturalist 128: 137–142. DOI: 10.1086/284547.
Paez, D.J., Morrissey, M., Bernatchez, L. & Dodson, J.J. (2010). The genetic basis of early-life morphological traits and their relation to alternative male reproductive tactics in Atlantic salmon. Journal of Evolutionary Biology 23: 757–768. DOI: 10.1111/j.1420-9101.2010.01941.x.
Petersson, E. & Järvi, T. (1993) Differences in reproductive traits between sea-ranched andwild sea-trout (Salmo trutta) originating from a common stock. Nordic Journal of Freshwater Research 68: 91–97.
Petersson, E., Järvi, T., Steffner, N.G. & Ragnarsson, B. (1996) The effect of domestication on some life history traits of sea trout (Salmo trutta) and Atlantic salmon (S. salar). Journal of Fish Biology 48: 776–791. DOI: 10.1111/j.1095-8649.1996.tb01471.x.
Pitcher, T.E., Neff, B.D., Rodd, F.H. & Rowe, L. (2003). Multiple mating and sequential mate choice in guppies: females trade up. Proceedings of the Royal Society of London B 270: 1623–1629. DOI: 10.1098/rspb.2002.2280.
Roff, D.A. (2000). Trade-offs between growth and reproduction: an analysis of the quantitative genetic evidence. Journal of Evolutionary Biology 13: 434–445. DOI: 10.1046/j.1420-9101.2000.00186.x.
Roff, D.A. (2015). Phylogenetic analysis of the evolution of semelparity. In T. Vladić, E. Petersson (Eds.), Evolutionary Biology of the Atlantic Salmon (pp. 248–257). Taylor and Francis, CRC Press.
Rolf, J.F. & Sokal, R.R. (2012). Statistical tables. W.H. Freeman and Company, New York.
Rudolfsen, G., Figenschou, L., Folstad, I., Tveuten, H. & Figenschou, M. (2006). Rapid adjustments of sperm characteristics in relation to social status. Proceedings of the Royal Society of London B 273: 325–332. DOI: 10.1098/rspb.2005.3305.
Salminen, M. (1997) Relationships between smolt size, postsmolt growth and sea age at maturity in Atlantic salmon ranched in the Baltic Sea. Journal of Applied Ichthyology 13: 121–130. DOI: 10.1111/j.1439-0426.1997.tb00111.x.
Schűtz, D. Pachler, G., Ripmeester, E., Goffinet, O. & Taborsky, M. (2010). Reproductive investment of giants and dwarfs: specialized tactics in a cichlid fish with alternative male morphs. Functional Ecology 24: 131–140. DOI: 10.1111/j.1365-2435.2009.01605.x.
Sibly, R.M. & Calow, P. (1986). Physiological ecology of animals. Blackwell.
Simmons, L.W. & Emlen, D.J. (2006). Evolutionary trade-off between weapons and testes. Proceedings of the National Academy of Sciences USA 103: 16346–16351. DOI: 10.1073/pnas.0603474103.
Stearns, S.C. (1989). Trade-offs in life-history evolution. Functional Ecology 3: 259–268. DOI: 10.2307/2389364.
Stearns, S.C. (1992). The Evolution of Life Histories. Oxford University press.
Thorpe, J.E., Mangel, M., Metcalfe, N.B. & Huntingford, F.A. (1998). Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. Evolutionary Ecology 12: 581–599. DOI: 10.1023/A:1022351814644.
Tomkins, J.L. & Hazel, W. (2008). The status of conditional evolutionary stable strategy. Trends in Ecology and Evolution 22: 522–528. DOI: 10.1016/j.tree.2007.09.002.
Tomkins, J. & Simmons, L.W. (2002). Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Animal Behaviour 63: 1009–1016.
Tremblay, G. & Giguère, L.A. (1992). Relation longueur/écaille allométrque chez le saumon atlantique (Salmo salar) durant la phase marine. Canadian Journal of Fisheries and Aquatic Sciences 49: 46–51. DOI: 10.1139/f92-005.
Vladić T. (2001). Gonad and Ejaculate Allocation in Alternative Reproductive Tactics of Salmon and Trout with Reference to Sperm Competition. Unpublished doctoral dissertation, Stockholm University, Stockholm. URN: urn:nbn:se:su:diva-71969.
Vladić, T.V. & Järvi, T. (2001). Sperm quality in alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle. Proceedings of the Royal Society of London B 268: 2375–2381. DOI: 10.1098/rspb.2001.1768.
Vladić, T.V., Afzelius, B.A. & Bronnikov, G.E. (2002). Sperm quality as reflected through morphology in salmon alternative life histories. Biology of Reproduction 66: 98–105. DOI: 10.1095/biolreprod66.1.98.
Vladić, T., Forsberg, L.A. & Järvi, T. (2010) Sperm competition between alternative reproductive tactics of the Atlantic salmon in vitro. Aquaculture 302: 265–269. DOI: 10.1016/j.aquaculture.2010.02.024.
Vladić, T. & Petersson, E. (2015). Relationship between size, age and maturity in the Atlantic Salmon. In T. Vladić & E. Petersson (Eds.), Evolutionary Biology of the Atlantic Salmon (pp. 165–182). Taylor and Francis, CRC Press. DOI: 10.1201/b18721-11.

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