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The Mating System of Steelhead, Oncorhynchus mykiss, Inferred by Molecular Analysis of Parents and Progeny

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Abstract

The development of molecular markers has allowed behavioral ecologists to link parents to specific offspring, providing insights into breeding systems that were not apparent from direct observations of the social system. Studies of this type in fishes have focused on species with male parental care such as centrarchids, and on salmonids, a family with little parental care. In order to gain further insight into the mating system of steelhead trout, Oncorhynchus mykiss, a winter-spawning species whose reproductive system is poorly known, adults returning to spawn were captured in four consecutive years in a small, unfished, wild population. Juvenile offspring were sampled by electrofishing and parentage was determined by exclusion based on a 12 locus microsatellite genotype. Both males and females mated with multiple individuals, though single pair matings were also inferred. Females and males tended to have the same number of mates (median = 1), but males were more likely to have no apparent partner (43% vs. 23% for females) and the maximum number of mates were obtained by males (range 0–10 vs. 0–5 for females). There was no difference in median arrival date by sex, but 80% of the females mated with males that had already arrived rather than males arriving with or after the females (median = 7.5, range = 1–63 days difference). Contrary to expectations, there was no evidence of size-assortative mating; larger males and larger females did not tend to mate with each other more often than would have occurred by chance. Of the juveniles with only one identified parent, most had a known mother and an unknown father rather than the reverse (88% vs. 11%). We interpret this as indirect evidence that non-anadromous males achieved a significant number of fertilizations. Thus the steelhead mating system was complex, being more strongly structured by arrival date than fish size, and including a significant genetic contribution by mature male parr.

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References

  • Ardren, W.R., S. Borer, F. Thrower, J.E. Joyce & A.R. Kapuscinski. 1999. Inheritance of 12 microsatellite loci in Oncorhynchus mykiss. J. Hered. 90: 529–536.

    Article  CAS  Google Scholar 

  • Ardren, W.R. & A.R. Kapuscinski. 2003. Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout. Mol. Ecol. 12: 35–49.

    Article  CAS  Google Scholar 

  • Baker, J., P. Bentzen & P. Moran. 2002. Molecular markers distinguish coastal cutthroat trout from coastal rainbow trout/steelhead and their hybrids. Trans. Amer. Fish. Soc. 131: 404–417.

    Article  CAS  Google Scholar 

  • Beacham, T.D. & C.B. Murray. 1993. Fecundity and egg size variation in North American Pacific salmon (Oncorhynchus). J. Fish Biol. 42: 485–508.

    Article  Google Scholar 

  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme. 2000. GENETIX 4.02, logiciel sous Windows™ pour la genetique des populations, University of Montpellier II, Laboratoire de Populations, Montpellier, France.

    Google Scholar 

  • Bentzen, P., J.B. Olsen, J.E. McLean, T.R. Seamons & T.P. Quinn. 2001. Kinship analysis of Pacific salmon: Insights into mating, homing, and timing of reproduction. J. Hered. 92: 127–136.

    Article  CAS  Google Scholar 

  • Berejikian, B.A., E.P. Tezak & A.L. LaRae. 2000. Female mate choice and spawning behavior of chinook salmon under experimental conditions. J. Fish Biol. 57: 647–661.

    Article  Google Scholar 

  • Birkhead, T.R., T. Burke, R. Zann, F.M. Hunter & A.P. Krupa. 1990. Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting. Behav. Ecol. Sociobiol. 27: 315–324.

    Article  Google Scholar 

  • Birkhead, T.R. & A.P. Møller. 1998. Sperm Competition and Sexual Selection, Academic Press, London. 826 pp.

    Google Scholar 

  • Busby, P.J., T.C. Wainwright, G.J. Bryant, L. Lierheimer, R.S. Waples, F.W. Waknitz & I.V. Lagomarsino. 1996. Status review of west coast steelhead from Washington, Idaho, Oregon, and California. NOAA Tech. Memo., U.S. Dep. Commer. NMFS-NWFSC-27. 261 pp.

  • Chebanov, N.A., N.V. Varnavskaya & V.S. Varnavskiy. 1983. Effectiveness of spawning of male sockeye salmon Oncorhynchus nerka (Salmonidae), of differing hierarchical rank by means of genetic-biochemical markers. J. Ichthyol. 23: 51–55.

    Google Scholar 

  • de Gaudemar, B., J.M. Bonzom & E. Beall. 2000. Effects of courtship and relative mate size on sexual motivation in Atlantic salmon. J. Fish Biol. 57: 502–515.

    Article  Google Scholar 

  • DeWoody, J.A. & J.C. Avise. 2001. Genetic perspectives on the natural history of fish mating systems. J. Hered. 92: 167–172.

    Article  CAS  Google Scholar 

  • Dickerson, B.R., T.P. Quinn & M.F. Willson. 2002. Body size, arrival date, and reproductive success of pink salmon, Oncorhynchus gorbuscha. Ethol. Ecol. Evol. 14: 29–44.

    Google Scholar 

  • Emlen, S.T. & L.W. Oring. 1977. Ecology, sexual selection, and the evolution of mating systems. Science 197: 215–223.

    CAS  Google Scholar 

  • Fields, R.D., K.R. Johnson & G.H. Thorgaard. 1989. DNA fingerprints in rainbow trout detected by hybridization with DNA of bacteriophage M13. Trans. Amer. Fish. Soc. 118: 78–81.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Foote, C.J. 1988. Male mate choice dependent on male size in salmon. Behaviour 106: 63–80.

    Google Scholar 

  • Foote, C.J. 1989. Female mate preference in Pacific salmon. Anim. Behav. 38: 721–722.

    Google Scholar 

  • Foote, C.J. 1990. An experimental comparison of male and female spawning territoriality in a Pacific salmon. Behaviour 115: 283–314.

    Google Scholar 

  • Foote, C.J., G.S. Brown & 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.

    Article  Google Scholar 

  • Garant, D., J.J. Dodson & L. Bernatchez. 2001. A genetic evaluation of mating system and determinants of individual reproductive success in Atlantic salmon (Salmo salar L.). J. Hered. 92: 137–145.

    Article  CAS  Google Scholar 

  • Gjerde, B. 1986. Growth and reproduction in fish and shellfish. Aquaculture 57: 37–55.

    Google Scholar 

  • Gross, M.R. 1985. Disruptive selection for alternative life histories in salmon. Nature 313: 47–48.

    Article  Google Scholar 

  • Hanson, A.J. & H.D. Smith. 1967. Mate selection in a population of sockeye salmon (Oncorhynchus nerka) of mixed age-groups. J. Fish. Res. Board Can. 24: 1955–1977.

    Google Scholar 

  • Healey, M.C. & A. Prince. 1998. Alternative tactics in the breeding behaviour of male coho salmon. Behaviour 135: 1099–1124.

    Google Scholar 

  • Hughes, C. 1998. Integrating molecular techniques with field methods in studies of social behavior: A revolution results. Ecology 79: 383–399.

    Google Scholar 

  • Hutchings, J.A. & R.A. Myers. 1988. Mating success of alternative maturation phenotypes in male Atlantic salmon, Salmo salar. Oecologia 75: 169–174.

    Article  Google Scholar 

  • Jones, A.G. & J.C. Avise. 2001. Mating systems and sexual selection in male-pregnant pipefishes and seahorses: Insights from microsatellite-based studies of maternity. J. Hered. 92: 150–158.

    CAS  Google Scholar 

  • Keenleyside, M.H. A. & H.M.C. Dupuis. 1988. Courtship and spawning competition in pink salmon (Oncorhynchus gorbuscha). Can. J. Zool. 66: 262–265.

    Google Scholar 

  • Marshall, T.C., J. Slate, L.E.B. Kruuk & J.M. Pemberton. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7: 639–655.

    Article  CAS  Google Scholar 

  • Martinez, J.L., P. Moran, J. Perez, B. De Gaudemar, E. Beall & E. Garcia-Vazquez. 2000. Multiple paternity increases effective size of southern Atlantic salmon populations. Mol. Ecol. 9: 293–298.

    Article  CAS  Google Scholar 

  • Morán, P., A.M. Pendás, E. Beall & E. García-Vázquez. 1996. Genetic assessment of the reproductive success of Atlantic salmon precocious parr by means of VNTR loci. Heredity 77: 655–660.

    Google Scholar 

  • Morbey, Y. 2000. Protandry in Pacific salmon. Can. J. Fish. Aquat. Sci. 57: 1252–1257.

    Article  Google Scholar 

  • Needham, P.R. & A.C. Taft. 1934. Observations on the spawning of steelhead trout. Trans. Amer. Fish. Soc. 64: 333–338.

    Google Scholar 

  • 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 

  • Quinn, T.P. & C.J. Foote. 1994. The effects of body size and sexual dimorphism on the reproductive behavior of sockeye salmon, Oncorhynchus nerka. Anim. Behav. 48: 751–761.

    Google Scholar 

  • Raymond, M. & F. Rousset. 1995. An exact test for population differentiation. Evolution 49: 1280–1283.

    Google Scholar 

  • Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Google Scholar 

  • Schroder, S.L. 1981. The role of sexual selection in determining the overall mating patterns and mate choice in chum salmon. Ph.D. dissertation, University of Washington, Seattle, WA. 274 pp.

    Google Scholar 

  • Shapovalov, L. & A.C. Taft. 1954. Life histories of the steelhead rainbow trout (Salmo gairdneri gairdneri) and silver salmon (Oncorhynchus kisutch) with special reference to Waddell Creek, California, and recommendations regarding their management. Fish. Bull. 98: 375 pp.

    Google Scholar 

  • Sillero-Zubiri, C., D. Gottelli & D.W. Macdonald. 1996. Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav. Ecol. Sociobiol. 38: 331–340.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Steinberg, E.K., K.R. Lindner, J. Gallea, A. Maxwell, J. Meng & F.W. Allendorf. 2002. Rates and patterns of microsatellite mutations in pink salmon. Mol. Biol. Evol. 19: 1198–1202.

    CAS  Google Scholar 

  • Taggart, J.B., I.S. McLaren, D.W. Hay, J.H. Webb & 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.

    Article  CAS  Google Scholar 

  • Tautz, A.F. & C. Groot. 1975. Spawning behavior of chum salmon (Oncorhynchus keta) and rainbow trout (Salmo gairdneri). J. Fish. Res. Board Can. 32: 633–642.

    Google Scholar 

  • Tsiger, V.V., V.L. Skirin, N.I. Krupyanko, K.A. Kashlin & A.Y. Semenchenko. 1994. Life history form of male masu salmon (Oncorhynchus masou) in South Primor'e, Russia. Can. J. Fish. Aquat. Sci. 51: 197–208.

    Google Scholar 

  • Unwin, M.J., M.T. Kinnison & T.P. Quinn. 1999. Exceptions to semelparity: Postmaturation survival, morphology, and energetics of male chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci. 56: 1172–1181.

    Article  Google Scholar 

  • Weir, B.S. & C.C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.

    Google Scholar 

  • Westneat, D. 1987. Extra-pair fertilizations in a predominantly monogamous birds: Genetic evidence. Anim. Behav. 35: 877–886.

    Google Scholar 

  • Young, W.P., C.O. Ostberg, P. Keim & G.H. Thorgaard. 2001. Genetic characterization of hybridization and introgression between anadromous rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki). Mol. Ecol. 10: 921–930.

    Article  CAS  Google Scholar 

  • Zar, J.H. 1999. Biostatistical Analysis, Prentice Hall, Upper Saddle River, New Jersey. 663 pp.

    Google Scholar 

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Seamons, T.R., Bentzen, P. & Quinn, T.P. The Mating System of Steelhead, Oncorhynchus mykiss, Inferred by Molecular Analysis of Parents and Progeny. Environmental Biology of Fishes 69, 333–344 (2004). https://doi.org/10.1023/B:EBFI.0000022893.88086.8f

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