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Effect of parental phenotype on dispersal, growth and maturation of offspring in wild masu salmon (Oncorhynchus masou)

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Abstract

Offspring traits are influenced by complex interactions among parent genotypes and phenotypes. However, ecological studies of these effects have tended to focus on one of either maternal or paternal influences. In this study, we investigated the effects of both parental phenotypes on offspring dispersal, growth and early sexual maturity in masu salmon. We used wild-caught parental fish in a half-sib mating design that allowed comparison of offspring from males of two different life-history types (precocious males that had lived only in fresh water and anadromous males that had migrated to the sea). These males were mated with anadromous females and the eggs planted in natural streams in three different years. Natal dispersal distance depended on offspring sex, body size and paternal life history: female offspring moved further downstream than males, whilst daughters of precocious fathers tended to move further downstream than those of anadromous sires. There was a maternal effect on offspring growth, with larger eggs resulting in larger offspring at least until these became precociously mature at the end of the first summer. However, while faster growing male offspring were more likely to become precociously mature, there was no evidence that the probability of precocious maturation was influenced by parental life history. We conclude that, although body size of young salmon was significantly influenced by egg size and there were sex differences in dispersal, their growth rate and divergence in life history types were mainly environmentally driven.

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References

  • Aich U, Jennions MD, Fox RJ (2020) An experimental test of the role of male mating history on paternal effects in the livebearer fish Gambusia holbrooki. Biol Lett 16:20190945

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson JH, Pess GR, Kiffney PM, Bennett TR, Faulds PL, Atlas WI, Quinn TP (2013) Dispersal and tributary immigration by juvenile coho salmon contribute to spatial expansion during colonization. Ecol Freshw Fish 22:30–42

    Article  Google Scholar 

  • Badyaev AV, Uller T (2009) Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc B Biol Sci 364:1169–1177

    Article  Google Scholar 

  • Baum D, Laughton R, Armstrong JD, Metcalfe NB (2004) Altitudinal variation in the relationship between growth and maturation rate in salmon parr. J Anim Ecol 73:253–260

    Article  Google Scholar 

  • Beacham TD, Murray CB (1985) Effect of female size, egg size, and water temperature on developmental biology of chum salmon (Oncorhynchus keta) from the Nitinat River, British Columbia. Can J Fish Aquat Sci 42:1755–1765

    Article  Google Scholar 

  • Berejikian BA, Van Doornik DM, Atkins JJ (2011) Alternative male reproductive phenotypes affect offspring growth rate in Chinook salmon. Trans Am Fish Soc 140:1206–1212

    Article  Google Scholar 

  • Bradford MJ, Taylor GC (1997) Individual variation in dispersal behaviour of newly emerged Chinook salmon (Oncorhynchus tshawytscha) from the upper Fraser River, British Columbia. Can J Fish Aquat Sci 54:1585–1592

    Article  Google Scholar 

  • Burton T, Mckelvey S, Stewart DC, Armstrong JD, Metcalfe NB (2013) Early maternal experience shapes offspring performance in the wild. Ecology 94:618–626

    Article  PubMed  Google Scholar 

  • Crean AJ, Bonduriansky R (2014) What is a paternal effect? Trends Ecol Evol 29:554–559

    Article  PubMed  Google Scholar 

  • Dobson FS (2013) The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution. Anim Behav 85:299–304

    Article  Google Scholar 

  • Dodson JJ, Aubin-Horth N, Thériault V, Páez DJ (2013) The evolutionary ecology of alternative migratory tactics in salmonid fishes. Biol Rev 88:602–625

    Article  PubMed  Google Scholar 

  • Eilertsen EM, Bårdsen BJ, Lijedal S, Rudolfsen G, Folstad I (2009) Experimental evidence for paternal effects on offspring growth rate in Arctic charr (Salvelinus alpinus). Proc R Soc B Biol Sci 276:129–136

    Article  Google Scholar 

  • Einum S, Fleming IA (1999) Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proc R Soc B Biol Sci 266:2095–2100

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Einum S, Finstad AG, Robertsen G, Nislow KH, McKelvey S, Armstrong JD (2012) Natal movement in juvenile Atlantic salmon: a body size-dependent strategy? Popul Ecol 54:285–294

    Article  Google Scholar 

  • Evans JP, Kelley JL, Bisazza A, Finazzo E, Pilastro A (2004) Sire attractiveness influences offspring performance in guppies. Proc R Soc B Biol Sci 271:2035–2042

    Article  Google Scholar 

  • Evans JP, Rahman MM, Gasparini C (2015) Genotype-by-environment interactions underlie the expression of pre- and post-copulatory sexually selected traits in guppies. J Evol Biol 28:959–972

    Article  CAS  PubMed  Google Scholar 

  • Falica BK, Lehnert SJ, Pitcher TE, Heath DD, Higgs DM (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 IA, Gross MR (1990) Latitudinal clines: a trade-off between egg number and size in Pacific salmon. Ecology 71:1–11

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Fox CW, Czesak ME, Wallin WG (2004) Complex genetic architecture of population differences in adult lifespan of a beetle: nonadditive inheritance, gender differences, body size and a large maternal effect. J Evol Biol 17:1007–1017

    Article  CAS  PubMed  Google Scholar 

  • Friedland KD, Haas RE (1996) Marine post-smolt growth and age at maturity of Atlantic salmon. J Fish Biol 48:1–15

    Article  Google Scholar 

  • Gjerde B, Simianer H, Refstie T (1994) Estimates of genetic and phenotypic parameters for body weight, growth rate and sexual maturity in Atlantic salmon. Livest Prod Sci 38:133–143

    Article  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  CAS  PubMed  Google Scholar 

  • Heath DD, Fox CW, Heath JW (1999) Maternal effects on offspring size: variation through early development of Chinook salmon. Evolution 53:1605–1611

    Article  PubMed  Google Scholar 

  • Heino M, Dieckmann U, Godø OR (2002) Measuring probabilistic reaction norms for age and size at maturation. Evolution 56:669–678

    PubMed  Google Scholar 

  • Johnston TA (1997) Downstream movements of young-of-the-year fishes in Catamaran Brook and the Little Southwest Miramichi River, New Brunswick. J Fish Biol 51:1047–1062

    Article  Google Scholar 

  • Kahler TH, Roni P, Quinn TP (2001) Summer movement and growth of juvenile anadromous salmonids in small western Washington streams. Can J Fish Aquat Sci 58:1947–1956

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Kitanishi S, Yamamoto T, Ishii H, Yamaguchi Y, Kobayashi T (2017) Dispersal patterns of anadromous and freshwater resident masu salmon at different spatial scales in mid-western Hokkaido, Japan. Ichthyol Res 64:111–115

    Article  Google Scholar 

  • Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86:692–716

    Article  PubMed  Google Scholar 

  • Kruuk LEB, Livingston J, Kahn A, Jennions MD (2015) Sex-specific maternal effects in a viviparous fish. Biol Lett 11:20150472

    Article  PubMed  PubMed Central  Google Scholar 

  • Lillehammer M, Ødegård J, Madsen P, Gjerde B, Refstie T, Rye M (2013) Survival, growth and sexual maturation in Atlantic salmon exposed to infectious pancreatic necrosis: a multi-variate mixture model approach. Genet Sel Evol 45:8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobon-Cervia J, Utrilla CG, Rincón PA, Amezcua F (1997) Environmentally induced spatio-temporal variations in the fecundity of brown trout Salmo trutta L.: trade-offs between egg size and number. Freshw Biol 38:277–288

    Article  Google Scholar 

  • Marshall DJ, Heppell SS, Munch SB, Warner RR (2010) The relationship between maternal phenotype and offspring quality: Do older mothers really produce the best offspring? Ecology 91:2862–2873

    Article  PubMed  Google Scholar 

  • Mayama H (1989) Sexual difference in spatial distribution of hatchery-reared juvenile masu salmon, Oncorhynchus masou, planted into stream. Sci Rep Hokkaido Salmon Hatch 43:115–118

    Google Scholar 

  • Metcalfe NB, Thorpe JE (1992) Early predictors of life-history events: the link between first feeding date, dominance and seaward migration in Atlantic salmon, Salmo salar L. J Fish Biol 41:93–99

    Article  Google Scholar 

  • Monaghan P, Maklakov AA, Metcalfe NB (2020) Intergenerational transfer of ageing: parental age and offspring life span. Trends Ecol Evol 35:927–937

    Article  PubMed  Google Scholar 

  • Morita K, Yamamoto S (2001) Contrasts in movement behavior of juvenile white-spotted charr between stocks above and below a dam. Fish Sci 67:179–181

    Article  CAS  Google Scholar 

  • Morita K, Tsuboi J, Nagasawa T (2009) Plasticity in probabilistic reaction norms for maturation in a salmonid fish. Biol Lett 5:628–631

    Article  PubMed  PubMed Central  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13(10):403–407

    Article  CAS  PubMed  Google Scholar 

  • Nagata M, Irvine JR (1997) Differential dispersal patterns of male and female masu salmon fry. J Fish Biol 51:601–606

    Article  Google Scholar 

  • Páez DJ, Morrissey M, Bernatchez L, Dodson JJ (2010) The genetic basis of early-life morphological traits and their relation to alternative male reproductive tactics in Atlantic salmon. J Evol Biol 23:757–768

    Article  PubMed  Google Scholar 

  • Perrin N, Mazalov V (1999) Dispersal and inbreeding avoidance. Am Nat 154:282–292

    Article  PubMed  Google Scholar 

  • Piché J, Hutchings JA, Blanchard W (2008) Genetic variation in threshold reaction norms for alternative reproductive tactics in male Atlantic salmon, Salmo salar. Proc R Soc B Biol Sci 275(1642):1571–1575

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

  • Ricker WE (1975) Computation and interpretation of biological statistics of fish populations. Bull Fish Res Board Can 191:1–382

    Google Scholar 

  • Segers FHID, Berishvili G, Taborsky B (2012) Egg size-dependent expression of growth hormone receptor accompanies compensatory growth in fish. Proc R Soc B Biol Sci 279:592–600

    Article  CAS  Google Scholar 

  • Taborsky M (2001) The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J Hered 92:100–110

    Article  CAS  PubMed  Google Scholar 

  • Thorn MW, Morbey YE (2017) Egg size and the adaptive capacity of early life history traits in Chinook salmon (Oncorhynchus tshawytscha). Evol Appl 11:205–219

    Article  PubMed  PubMed Central  Google Scholar 

  • Thorpe JE, Morgan RIG, Talbot C, Miles MS (1983) Inheritance of developmental rate in Atlantic salmon, Salmo salar L. Aquaculture 33:119–128

    Article  Google Scholar 

  • Tschirren B, Fitze PS, Richner H (2007) Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am Nat 169:87–93

    Article  PubMed  Google Scholar 

  • Van Leeuwen TE, McLennan D, McKelvey S, Stewart DC, Adams CE, Metcalfe NB (2016) The association between parental life history and offspring phenotype in Atlantic salmon. J Exp Biol 219:374–382

    PubMed  Google Scholar 

  • Wirtz-Ocaňa S, Schutz D, Pachler G, Taborsky M (2013) Paternal inheritance of growth in fish pursuing alternative reproductive tactics. Ecol Evol 3:1614–1625

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamamoto T, Edo K (2002) Reproductive behaviors related to life history forms in male masu salmon, Oncorhynchus masou Brevoort, in Lake Toya, Japan. J Freshw Ecol 17:275–281

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank T. Endo, T. Nishio, H. Omiya and C. Uehara for help with the parental crosses, and M. Komiya, M. Koshimi and A. Ohya for their help in the field. We are grateful K. Etoh and N. Yoshida for assistance in DNA analysis in the laboratory. Two referees made very helpful comments on an earlier version of the manuscript. We thank Nippon Veterinary and Life Science University for funding TY’s sabbatical visit at the University of Glasgow. This study was supported in part by JSPS Grants-in-Aid for Scientific Research 25430196.

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T.Y., S.K. and N.B.M. conceived the ideas for the manuscript; T.Y. and S.K. led the project and designed methodology; T.Y. and N.B.M. led the writing of the manuscript and S.K. provided data. All authors contributed critically to the drafts and gave final approval for publication.

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Correspondence to Toshiaki Yamamoto.

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Yamamoto, T., Kitanishi, S. & Metcalfe, N.B. Effect of parental phenotype on dispersal, growth and maturation of offspring in wild masu salmon (Oncorhynchus masou). Evol Ecol 35, 253–269 (2021). https://doi.org/10.1007/s10682-020-10098-2

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