Skip to main content
Log in

Paternal body size affects reproductive success in laboratory-held zebrafish (Danio rerio)

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Across many fish species, large females tend to exhibit higher individual reproductive success due to elevated fecundity and the provisioning of better conditioned eggs and offspring compared to small females. By contrast, effects of paternal body size on reproductive success are less well understood. We disentangled the maternal- and paternal-size dependent effects on reproductive output and early life history in zebrafish (Danio rerio). In the laboratory, females and males from four size categories (small, medium-sized, large and very large) were allowed to spawn freely in a full factorial design with 10 replicates per size combination. As expected, larger females produced more eggs and better conditioned offspring compared to smaller females. Male body size further contributed to zebrafish reproductive success: offspring sired by large males exhibited higher hatching probability and these offspring also hatched earlier and larger than offspring fertilized by small males. However, the largest males experienced lower mating success and received fewer eggs than males of the smaller size classes. While male body size substantially affected reproductive success in zebrafish, it remained unclear whether and to what degree direct paternal effects (e.g., related to sperm quality) or indirect paternal effects stemming from differential allocation patterns by females were the mechanism behind our findings. Answering this question constitutes an important future research topic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alderdice DF (1988) Osmotic and ionic regulation in teleost eggs and larvae. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic, London

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press

  • Bang A, Grønkjær P, Clemmsen C, Høie H (2006) Parental effects on early life history traits of Atlantic herring (Clupea harengus L.) larvae. J Exp Mar Biol Ecol 334:51–63

    Article  Google Scholar 

  • Bernardo J (1996) Maternal effects in animal ecology. Amer Zool 36:83–105

    Google Scholar 

  • Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132:611–628

    Article  Google Scholar 

  • Chambers RC, Leggett WC (1996) Maternal influences on variation in egg sizes in temperate marine fishes. Amer Zool 63:180–196

    Google Scholar 

  • Chambers RC, Leggett WC, Brown JA (1989) Egg size, female effects, and the correlation between early life history traits in capelin, Mallotus villosus: an appraisal at the individual level. Fish Bull 87:515–523

    Google Scholar 

  • Crawley RJ (2007) The R book. Wiley, West Sussex

    Book  Google Scholar 

  • Danzmann RG, Ferguson MM, Allendorf FW (1989) Genetic variability and components of fitness in hatchery strains of rainbow trout. J Fish Biol 35(supplA):313–319

    Google Scholar 

  • Eaton RC, Farley RD (1974) Spawning cycle and egg production of zebrafish, Brachydanio rerio, in the laboratory. Copeia 1974:195–204

    Article  Google Scholar 

  • Fowler K, Partridge L (1989) A cost of mating in female fruitflies. Nature 338:760–761

    Article  Google Scholar 

  • Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JP, Parker GA (2004) Spermatozoa traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47

    PubMed  CAS  Google Scholar 

  • Gerlach G, Lysiak N (2006) Kin recognition and inbreeding avoidance in zebrafish, Danio rerio, is based on phenotype matching. Anim Behav 71:1371–1377

    Article  Google Scholar 

  • Green BS (2008) Maternal effects in fish populations. Adv Mar Biol 54:1–105

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hisaoka KK, Firlit CF (1962) Ovarian cycle and egg production in the zebrafish, Brachydanio rerio. Copeia 1962:788–792

    Article  Google Scholar 

  • Howard RD, Martens RS, Innis SA, Drnevich JM, Hale J (1998) Mate choice and mate competition influence male body size in Japanese medaka. Anim Behav 55:1151–1163

    Article  PubMed  Google Scholar 

  • Hutter S, Penn DJ, Magee S, Zala SM (2010) Reproductive behaviour of wild zebrafish (Danio rerio) in large tanks. Behaviour 147:641–660

    Article  Google Scholar 

  • Jacob A, Nússle S, Britschgi A, Evanno G, Müller R, Wedekind C (2007) Male dominance linked to size and age but not to ‚good genes’ in brown trout (Salmo trutta). BMC Evol Biol 7:207

    Article  PubMed  Google Scholar 

  • Kamler E (2005) Parent-egg-progeny relationships in teleost fishes: an energetics perspective. Rev Fish Biol Fish 15:399–421

    Article  Google Scholar 

  • Kamler E (2008) Resource allocation in yolk-feeding fish. Rev Fish Biol Fish 57:789–796

    Google Scholar 

  • Kemadjou Njiwa JR, Müller P, Klein R (2004) Variations of sperm release in three batches of zebrafish. J Fish Biol 64:475–482

    Article  Google Scholar 

  • Kennedy J, Geffen AJ, Nash RDM (2007) Maternal influences on egg and larval characteristics of plaice (Pleuronectes platessa). J Sea Res 58:65–77

    Article  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dynam 18:143–200

    Google Scholar 

  • Kjørsvik E, Mangor-Jensen A, Holmefjord I (1990) Egg quality in fishes. Adv Mar Biol 26:71–113

    Article  Google Scholar 

  • Kolm N (2001) Females produce larger eggs for large males in a paternal mouthbrooding fish. Proc R Soc B 268:2229–2234

    Article  PubMed  CAS  Google Scholar 

  • Langangen Ø, Edeline E, Ohlberger J, Winfield IJ, Fletcher JM, James JB, Stenseth NC, Vøllestad LA (2011) Six decades of pike and perch population dynamics in Windermere. Fish Res 109:131–139

    Article  Google Scholar 

  • Marshall DJ, Allen RM, Crean AJ (2008) The ecological and evolutionary importance of maternal effects in the sea. Ocean Mar Biol Ann Rev 46:203–250

    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 

  • Marteinsdottir G, Steinarsson A (1998) Maternal influence on the size and viability of Icelandic cod Gadus morhua eggs and larvae. J Fish Biol 52:1241–1258

    Google Scholar 

  • McLean JE, Bentzen P, Quinn TP (2004) Does size matter? Fitness-related factors in steelhead trout determined by genetic parentage assignment. Ecology 85:2979–2985

    Article  Google Scholar 

  • Miller TJ, Crowder LB, Rice JA, Marshall EA (1988) Larval size and recruitment mechanisms in fishes: toward a conceptual framework. Can J Fish Aquat Sci 45:1657–1670

    Article  Google Scholar 

  • Morgan MJ, Wilson CE, Crim LW (1999) The effect of stress in reproduction in Atlantic cod. J F Biol 54:477–488

    Article  Google Scholar 

  • Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Partridge L, Fowler K (1990) Non-mating costs of exposure to males in female Drosophila melanogaster. J Insect Physiol 36:419–425

    Article  Google Scholar 

  • Paull GC, Van Look KJW, Santos EM, Filby AL, Gray DM, Nash JP, Tyler CR (2008) Variability in measures of reproductive success in laboratory-kept colonies of zebrafish and implications for studies addressing population-level effects of environmental chemicals. Aquatic Toxicology 87:115–126

    Article  PubMed  CAS  Google Scholar 

  • Paull GC, Filby AL, Giddins HG, Coe TS, Hamilton PB, Tyler CR (2010) Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success. Zebrafish 7:109–117

    Article  PubMed  CAS  Google Scholar 

  • Pitnick S, García-González F (2002) Harm to females increased with male body size in Drosophila melanogaster. Proc R Soc B 269:1821–1828

    Article  PubMed  Google Scholar 

  • Priestley SM, Stevenson AE, Alexander LG (2006) The influence of feeding frequency on growth and body condition of the common goldfish (Carassius auratus). J Nutr 136:1979S–1981S

    PubMed  CAS  Google Scholar 

  • Pritchard VL (2001) Behaviour and morphology of the zebrafish (Danio rerio). PhD Thesis, University of Leeds, Leeds, UK

  • Pyron M (2003) Female preferences and male-male interactions in zebrafish (Danio rerio). Can J Zool 81:122–125

    Article  Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. See http://www.R-project.org

  • Roff DA (2002) Life-history evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Sabat AM (1994) Mating success in brood-guarding male rock bass, Ambloplites rupestris: the effect of body size. Env Biol Fish 39:411–415

    Article  Google Scholar 

  • Saillant E, Chatain B, Fostier A, Przybyla C, Fauvel C (2001) Parental influence on early development in the European sea bass. J Fish Biol 58:1585–1600

    Article  Google Scholar 

  • Schilling TF (2002) The morphology of larval and adult zebrafish. In: Nüsslein-Vollhard C, Dahm R (eds) Zebrafish—A practical approach. Oxford University Press, Oxford

    Google Scholar 

  • Skinner AMJ (2004) Sexual selection in the zebra fish (Danio rerio) and the guppy (Poecilia reticulata). PhD Thesis, University of Sheffield, Sheffield, UK

  • Skinner AMJ, Watt PJ (2007a) Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata. Behav Ecol 18:47–52

    Article  Google Scholar 

  • Skinner AMJ, Watt PJ (2007b) Strategic egg allocation in the zebra fish, Danio rerio. Behav Ecol 18:905–909

    Article  Google Scholar 

  • Small BC (2004) Effect of dietary cortisol administration on growth and reproductive success on channel catfish. J Fish Biol 64:589–596

    Article  CAS  Google Scholar 

  • Spence R, Smith C (2005) Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish (Danio rerio). Anim Behav 69:1317–1323

    Article  Google Scholar 

  • Spence R, Smith C (2006) Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav Ecol 17:779–783

    Article  Google Scholar 

  • Spence R, Jordan WC, Smith C (2006) Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio. Front Zool 3:5

    Article  PubMed  Google Scholar 

  • Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev 83:13–34

    Article  PubMed  Google Scholar 

  • Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3:259–268

    Article  Google Scholar 

  • Thériault V, Moyer GR, Jackson LS, Blouin MS, Banks MA (2011) Reduced reproductive success of hatchery coho salmon in the wild: insights into most likely mechanisms. Mol Ecol 20:1860–1869

    Article  PubMed  Google Scholar 

  • Uusi-Heikkilä S, Wolter C, Meinelt T, Arlinghaus R (2010) Size-dependent reproductive success of wild zebrafish Danio rerio in the laboratory. J Fish Biol 77:552–569

    PubMed  Google Scholar 

  • Uusi-Heikkilä S, Kuparinen A, Wolter C, Meinelt T, O’Toole AC, Arlinghaus R (2011) Experimental assessment of the probabilistic maturation reaction norm: condition matters. Proc R Soc B 278:709–717

    Article  PubMed  Google Scholar 

  • van den Hurk R, Lambert JGD (1983) Ovarian steroid glucuronides function as sex pheromones for male zebrafish, Brachydanio rerio. Can J Zool 61:2381–2387

    Article  Google Scholar 

  • van den Hurk R, Schoonen WGEJ, van Zoelen GA, Lambert JGD (1987) The biosynthesis of steroid glucuronides in the testis of the zebrafish, Brachydanio rerio, and their pheromonal function as ovulation inducers. Gen Comp Endocrinol 68:179–188

    Article  PubMed  Google Scholar 

  • Wootton RJ (1998) Ecology of teleost fishes, 2nd edn. Chapman & Hall, London

    Google Scholar 

Download references

Acknowledgments

Funding for this study was through the Adaptfish Project grant to RA and CW by the Gottfried-Wilhelm-Leibniz-Community (www.adaptfish.igb-berlin.de) and through the Academy of Finland for AK. We thank Sarah Becker and Amanda O’Toole for help in collecting the data and in husbandry of zebrafish. Additionally, we thank Thomas Mehner and the participants of the course on Scientific Writing at IGB for helpful discussion on an earlier draft of this article, and four reviewers for feedback. The finalization of this study was financially supported by the project Besatzfisch (www.besatz-fisch.de) by the German Ministry for Education and Research in the Program on Social-Ecological Research (grant # 01UU0907, www.besatz-fisch.de).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Uusi-Heikkilä.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Uusi-Heikkilä, S., Kuparinen, A., Wolter, C. et al. Paternal body size affects reproductive success in laboratory-held zebrafish (Danio rerio). Environ Biol Fish 93, 461–474 (2012). https://doi.org/10.1007/s10641-011-9937-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-011-9937-5

Keywords

Navigation