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Effect of paternal life-history form and egg size on offspring life-history traits in masu salmon Oncorhynchus masou

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Abstract

To clarify the effect of paternal life-history form and egg size on offspring life-history traits (e.g., growth and maturation) in masu salmon (Oncorhynchus masou), we studied an artificially fertilized population for 3 years using mark-recapture methods. The body size of offspring in early life was associated with egg size, but not paternal life-history form. By contrast, the growth rate of individuals during summer and winter seasons was not influenced by egg size or paternal life-history form. Movement within the tributary differed between males and females, with more females moving downstream during early life stages compared to males. However, the effects of egg size and paternal life-history form on the movement of offspring were not detected. Out of 192 males that remained in the tributary, 77 had relatively large body sizes and reached sexual maturity at one year old. The probability of maturation was associated with the body size in September, but not with paternal life-history form and egg size. We concluded that offspring life-history traits are profoundly influenced by environmental conditions, whereas they are slightly influenced by parental genetic effects.

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Data availability

The datasets generated during the current study are available from the authors upon reasonable request.

References

  • Achord, S., R. W. Zabel & B. P. Sandford, 2007. Migration timing, growth and estimated parr-to-smolt survival rates of wild Snake River spring-summer Chinook salmon from the Salmon River basin, Idaho, to the lower Snake River. Transaction of the American Fisheries Society 136: 142–154.

    Article  Google Scholar 

  • Bates, D., M. Mächler, B. M. Bolker & S. C. Walker, 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67(1): 1–48.

    Article  CAS  Google Scholar 

  • Beckman, B. R., B. Gadberry, P. Parkins & D. A. Larsen, 2008. The Effect of Yakima River Spring Chinook Salmon Sire Life History Type on Emergence Timing and Size of Progeny. Transactions of the American Fisheries Society 137: 1285–1291.

    Article  Google Scholar 

  • Berejikian, B. A., D. M. Van Doornik & J. J. Atkins, 2011. Alternative male reproductive phenotypes affect offspring growth rate in Chinook salmon. Transactions of the American Fisheries Society 140: 1206–1212.

    Article  Google Scholar 

  • Bochdansky, A. B., P. Gronkjaer, T. P. Herra & W. C. Leggett, 2005. Experimental evidence for selection against fish larvae with high metabolic rates in a food limited environment. Marine Biology 147: 1413–1417.

    Article  Google Scholar 

  • Bouchard, C., F. Lange, F. Guéraud, J. Rives & C. Tentelier, 2020. Sexual maturity increases mobility and heterogeneity in individual space use in Atlantic salmon (Salmo salar) Parr. Journal of Fish Biology 96: 925–938.

    Article  PubMed  Google Scholar 

  • Brooks, S., C. R. Tyler & J. P. Sumpter, 1997. Egg quality in fish: What makes a good egg? Reviews in Fish Biology and Fisheries 7: 387–416.

    Article  Google Scholar 

  • Burton, T., S. McKelvey, D. C. Stewart, J. D. Armstrong & N. B. Metcalfe, 2013. Early maternal experience shapes offspring performance in the wild. Ecology 94: 618–626.

    Article  PubMed  Google Scholar 

  • Burton, T., N. Rollinson, S. McKelvey, D. C. Stewart, J. D. Armstrong & N. B. Metcalfe, 2020. Adaptive maternal investment in the wild? Links between maternal growth trajectory and offspring size, growth and survival in contrasting environments. The American Naturalist 195: 678–690.

    Article  PubMed  Google Scholar 

  • Crean, A. J. & R. Bonduriansky, 2014. What is a paternal effect? Trends in Ecology and Evolution 29: 554–559.

    Article  PubMed  Google Scholar 

  • Cutts, C. J., N. B. Metcalfe & A. C. Taylor, 1998. Aggression and growth depression in Juvenile salmon- the consequences of variation in metabolic rate. Journal of Fish Biology 52: 1026–1037.

    Article  Google Scholar 

  • Einum, S. & I. A. Fleming, 1999. Maternal effects of egg size in brown trout (Salmo trutta): Norms of reaction to environmental quality. Proceedings of the Royal Society b: Biological Sciences 266: 2095–2100.

    Article  PubMed Central  Google Scholar 

  • Einum, S. & I. A. Fleming, 2000. Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution 54: 628–639.

    Article  CAS  PubMed  Google Scholar 

  • Engqvist, L. & M. Taborsky, 2016. The evolution of genetic and conditional alternative reproductive tactics. Proceedings of the Royal Society b: Biological Sciences 283: 20152945.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Falica, B. K., S. J. Lehnert, T. E. Pitcher, D. D. Heath & D. M. Higgs, 2017. Ontogenetic shifts in genetic and maternal effects on length and survival in Chinook salmon (Oncorhynchus tshawytscha). Aquaculture 468: 218–225.

    Article  Google Scholar 

  • Fleming, I. A., 1998. Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Canadian Journal of Fisheries and Aquatic Sciences 55: 59–76.

    Article  Google Scholar 

  • Fleming, I. A. & J. D. Reynolds, 2004. Salmonid breeding systems. In Hendry, A. P. & S. C. Stearns (eds), Evolution Illuminated: Salmon and Their Relatives Oxford University Press, Oxford: 264–294.

    Google Scholar 

  • Forest, A. R., M. G. E. Dender, T. E. Pitcher & C. A. D. Semeniuk, 2017. The effects of paternal reproductive tactic and rearing environment on juvenile variation in growth as mediated though aggression and foraging behaviours of Chinook salmon (Oncorhynchus tshawytscha). Ethology 123: 329–341.

    Article  Google Scholar 

  • Fox, C. W. & M. E. Czesak, 2000. Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45: 341–369.

    Article  CAS  PubMed  Google Scholar 

  • Garant, D., P.-M. Fontaine, S. P. Good, J. J. Dodson & L. Bernatchez, 2002. The influence of male parental identity on growth and survival of offspring in Atlantic salmon (Salmo salar). Evolutional Ecology Research 4: 537–549.

    Google Scholar 

  • Garant, D., J. J. Dodson & L. Bernatchez, 2003. Differential reproductive success and heritability of alternative reproductive tactics in wild Atlantic salmon (Salmo salar L.). Evolution 57: 1133–1141.

    PubMed  Google Scholar 

  • Gjerde, B., H. Simianer & T. Refstie, 1994. Estimates of genetic and phenotypic parameters for body weight, growth rate and sexual maturity in Atlantic salmon. Livestock Production Science 38: 133–143.

    Article  Google Scholar 

  • Heath, D. D. & D. M. Blouw, 1998. Are maternal effects in fish adaptive or merely physiological side effects? In Mousseau, T. A. & C. W. Fox (eds), Maternal Effects as Adaptations Oxford University Press, Oxford: 178–201.

    Google Scholar 

  • Heath, D. D., R. H. Devlin, J. W. Heath & G. K. Iwama, 1994. Genetic, environmental and interaction effects on the incidence of jacking in Oncorhynchus tshawytscha (Chinook salmon). Heredity 72: 146–154.

    Article  Google Scholar 

  • Heath, D. D., C. W. Fox & J. W. Heath, 1999. Maternal effects on offspring size: Variation through early development of Chinook salmon. Evolution 53: 1605–1611.

    Article  PubMed  Google Scholar 

  • Heath, D. D., L. Rankin, C. A. Bryden & J. W. Heath, 2002. Heritability and Y-chromosome influence in the jack male life history of chinook salmon (Oncorhynchus tshawytscha). Heredity 89: 311–317.

    Article  CAS  PubMed  Google Scholar 

  • Heggenes, J., K. Alfredsen, A. A. Bustos, A. Huusko & M. Stickler, 2018. Be cool: a review of hydropower-regulated northern streams. Environmental Biology of Fishes 101: 1–21.

    Article  Google Scholar 

  • Hurst, T. P., 2007. Causes and consequences of winter mortality in fishes. Journal of Fish Biology 71: 315–345.

    Article  Google Scholar 

  • Hutchings, J. A., 1991. Fitness consequences of variation in egg size and food abundance in brook trout Salvelinus fontinalis. Evolution 45: 1162–1168.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kato, F., 1991. Life histories of masu and amago salmon (Oncorhynchus masou and O. rhodurus). In Groot, C. & L. Margolis (eds), Pacific Salmon Life Histories University of British Columbia Press, Vancouver: 448–520.

    Google Scholar 

  • Koseki, Y. & K. Maekawa, 2002. Differential energy allocation of alternative male tactics in masu salmon (Oncorhynchus masou). Canadian Journal of Fisheries and Aquatic Sciences 59: 1717–1723.

    Article  Google Scholar 

  • Krist, M., 2011. Egg size and offspring quality: a meta-analysis in birds. Biological Reviews 86: 692–716.

    Article  PubMed  Google Scholar 

  • Kubo, T., 1974. Notes on the phase differentiation and smolt transformation of juvenile masu salmon (Oncorhynchus masou). Scientific Reports of the Hokkaido Salmon Hatchery 28: 9–26. (In Japanese, English summary)

  • Kuznetsova, A., P. B. Brockhoff & R. H. Bojesen-Christensen, 2016. ImerTest: Tests in linear Mixed Effects Models. http://CRAN.R-project.org/package=lmerTest

  • Marshall, D. J. & M. J. Keough, 2008. The evolutionary ecology of offspring size in marine invertebrates. Advances in Marine Biology 53: 1–60.

    Google Scholar 

  • Mayama, H., 1989. Sexual difference in spatial distribution of hatchery-reared juvenile masu salmon, Oncorhynchus masou, planted into stream. Scientific Reports of the Hokkaido Salmon Hatchery 43: 115–118 (In Japanese, English summary).

  • Metcalfe, N. B., 1998. The interaction between behavior and physiology in determining life history patterns in Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 55(suppl. 1): 93–103.

    Article  Google Scholar 

  • Metcalfe, N. B., A. C. Taylor & J. E. Thorpe, 1995. Metabolic rate, social status, and life history strategies in Atlantic salmon. Animal Behaviour 49: 431–436.

    Article  Google Scholar 

  • Morita, K., J. Tsuboi, G. Sahashi, T. Kikko, D. Ishizaki, D. Kishi, S. Endo & Y. Koseki, 2018. Iteroparity of stream resident masu salmon Oncorhynchus masou. Journal of Fish Biology 93: 750–754.

    Article  PubMed  Google Scholar 

  • Nagata, M. & J. R. Irvine, 1997. Differential dispersal patterns of male and female masu salmon fry. Journal of Fish Biology 51: 601–606.

    Article  Google Scholar 

  • Olsen, J. B., J. K. Wenburg & P. Bentzen, 1996. Semiautomated multilocus genotyping of Pacific salmon (Oncorhynchus spp.) using microsatellites. Molecular Marine Biology and Biotechnology 5: 259–272.

    CAS  PubMed  Google Scholar 

  • Olsen, J. B., S. L. Wilson, E. J. Kretschmer, K. C. Jones & J. E. Seeb, 2000. Characterization of 14 tetranucleotide microsatellite loci derived from sockeye salmon. Molecular Ecology 9: 2185–2187.

    Article  CAS  PubMed  Google Scholar 

  • Páez, D. J., M. Morrissey, L. Bernatchez & J. J. Dodson, 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.

    Article  PubMed  Google Scholar 

  • Palti, Y., R. G. Danzmann & C. E. Rexroad, 2003. Characterization and mapping of 19 polymorphic microsatellite markers for rainbow trout (Oncorhynchus mykiss). Animal Genetics 34: 153–156.

    Article  CAS  PubMed  Google Scholar 

  • Quinn, T. P., 2005. The Behavior and Ecology of Pacific Salmon and Trout, University of Washington Press, Washington:

    Google Scholar 

  • Qvarnström, A. & T. D. Price, 2001. Maternal effects, paternal effects and sexual selection. Trends in Ecology and Evolution 16: 95–100.

    Article  PubMed  Google Scholar 

  • R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Rexroad, C. E., R. L. Coleman, A. M. Martin, W. K. Hershberger & J. Killefer, 2001. Thirty-five polymorphic microsatellite markers for rainbow trout (Oncorhynchus mykliss). Animal Genetics 32: 317–319.

    Article  CAS  PubMed  Google Scholar 

  • Reznick, D. N., 1991. Maternal effects in fish life histories. In Dudley, E. (ed), Evolutionary Biology Discorides Press, Portland, OR: 780–793.

    Google Scholar 

  • Rhodes, J. S. & T. P. Quinn, 1998. Factors affecting the outcome of territorial contests between hatchery and naturally reared Coho salmon Parr in the laboratory. Journal of Fish Biology 53: 1220–1230.

    Article  Google Scholar 

  • Ricker, W. E., 1975. Computation and interpretation of biological statistics of fish populations. Bulletin of the Fisheries Research Board of Canada 191: 1–382.

    Google Scholar 

  • Rodriguez, F., C. E. Rexroad & Y. Palti, 2003. Characterization of twenty-four microsatellite markers for rainbow trout (Oncorhynchus mykiss). Molecular Ecology Notes 3: 619–622.

    Article  CAS  Google Scholar 

  • Rowe, D. K. & J. E. Thorpe, 1990. Differences in growth between maturing and non-maturing male Atlantic salmon (Salmo salar) Parr. Journal of Fish Biology 36: 643–658.

    Article  Google Scholar 

  • Segers, F. H. I. D., G. Berishvili & B. Taborsky, 2012. Egg size-dependent expression of growth hormone receptor accompanies compensatory growth in fish. Proceedings of the Royal Society b: Biological Sciences 279: 592–600.

    Article  CAS  PubMed  Google Scholar 

  • Thorgaard, G. H., 1977. Heteromorphic sex chromosomes in male rainbow trout. Science 196: 900–902.

    Article  CAS  PubMed  Google Scholar 

  • Thorn, M. W. & Y. E. Morbey, 2017. Egg size and the adaptive capacity of early life history traits in Chinook salmon (Oncorhynchus tshawytscha). Evolutionary Application 11: 205–219.

    Article  Google Scholar 

  • Thorpe, J. E., 1986. Age at maturity in Atlantic salmon, Salmo salar L.: fresh water period influence and conflicts with smolting. Canadian Special Publication of Fisheries and Aquatic Sciences 89: 7–14.

    Google Scholar 

  • Thorpe, J. E., R. I. G. Morgan, C. Talbot & M. S. Miles, 1983. Inheritance of developmental rate in Atlantic salmon, Salmo salar L. Aquaculture 33: 119–128.

    Article  Google Scholar 

  • Trotter, P. C., 1989. Coastal cutthroat trout: A life history compendium. Transactions of the American Fisheries Society 118: 463–473.

    Article  Google Scholar 

  • Utoh, H., 1976. Study of the mechanism of differentiation between the stream resident form and the seaward migratory form in masu salmon, Oncorhynchus masou Brevoort. Bulletin of the Faculty of Fisheries Hokkaido University 26: 321–326.

    Google Scholar 

  • Watanabe, M., S. Takamura & K. Maekawa, 2008. Effects of timing of nest entry and body size on the fertilization success of alternative male reproductive phenotypes of male salmon (Oncorhynchus masou). Canadian Journal of Zoology 86: 1121–1130.

    Article  Google Scholar 

  • Wirtz-Ocaňa, S., D. Schutz, G. Pachler & M. Taborsky, 2013. Paternal inheritance of growth in fish pursuing alternative reproductive tactics. Ecology and Evolution 3: 1614–1625.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolf, J. B. & M. J. Wade, 2009. What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B: Biological Sciences 364: 1107–1115.

  • Yamamoto, T., 2004. Sex-specific growth pattern during early life history in masu salmon Oncorhynchus masou. Ecology of Freshwater Fish 13: 203–207.

    Article  Google Scholar 

  • Yamamoto, T. & K. Edo, 2002. Reproductive behaviors related to life history forms in male masu salmon, Oncorhynchus masou Brevoort, in Lake Toya, Japan. Journal of Freshwater Ecology 17: 275–281.

    Article  Google Scholar 

  • Yamamoto, S. & S. Nakano, 1996. Growth and development of a bimodal length-frequency distribution during smolting in a wild population of white-spotted charr in northern Japan. Journal of Fish Biology 48: 68–79.

    Google Scholar 

  • Yamamoto, T., H. Ueda & S. Higashi, 1998. Correlation among dominance status, metabolic rate and otolith size in masu salmon. Journal of Fish Biology 52: 281–290.

    Article  Google Scholar 

  • Yamamoto, T., S. Kitanishi, M. Sato, M. Yagisawa & D. Kishi, 2021a. Links between paternal life history and offspring metabolic rate and body size during early life in masu salmon Oncorhynchus masou. Ecology of Freshwater Fish 30: 296–305.

    Article  Google Scholar 

  • Yamamoto, T., S. Kitanishi & N. B. Metcalfe, 2021b. Effect of parental phenotype on dispersal, growth and maturation of offspring in wild masu salmon (Oncorhynchus masou). Evolutionary Ecology 35: 253–269.

    Article  Google Scholar 

  • Yano, A., R. Guyomard, B. Nicol, E. Jouanno, E. Quillet, C. Klopp, C. Cabau, O. Bouchez & A. Fostier, 2012. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Current Biology 22: 1423–1428.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank M. Komiya, A. Ohya, T. Endo, and C. Uehara for their help in the field. We also thank Naho Yoshida and Kanako Eto for their assistance with DNA analysis.

Funding

This work was supported by the Japan Society for the Promotion of Science Grants-in-Aid for Scientific Research (Grant No. TY18K05796) and a Grant for Environmental Research from the Nissei Foundation, Japan.

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  1. Department of Veterinary Nursing and Technology, Nippon Veterinary and Life Science University, Musashino, Tokyo, Japan

    Toshiaki Yamamoto

  2. Faculty of Science and Technology, Oita University, 700 Dannoharu, Oita, Japan

    Shigeru Kitanishi

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  1. Toshiaki Yamamoto
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Correspondence to Toshiaki Yamamoto.

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Yamamoto, T., Kitanishi, S. Effect of paternal life-history form and egg size on offspring life-history traits in masu salmon Oncorhynchus masou. Hydrobiologia 849, 3149–3160 (2022). https://doi.org/10.1007/s10750-022-04922-9

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