Skip to main content
Log in

Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

  • Physiological ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Positive associations between maternal investment per offspring and maternal body size have been explained as adaptive responses by females to predictable, body size-specific maternal influences on the offspring’s environment. As a larger per-offspring investment increases maternal fitness when the quality of the offspring environment is low, optimal egg size may increase with maternal body size if larger mothers create relatively poor environments for their eggs or offspring. Here, we manipulate egg size and rearing environments (gravel size, nest depth) of Atlantic salmon (Salmo salar) in a 2 × 2 × 2 factorial experiment. We find that the incubation environment typical of large and small mothers can exert predictable effects on offspring phenotypes, but the nature of these effects provides little support to the prediction that smaller eggs are better suited to nest environments created by smaller females (and vice versa). Our data indicate that the magnitude and direction of phenotypic differences between small and large offspring vary among maternal nest environments, underscoring the point that removal of offspring from the environmental context in which they are provisioned in the wild can bias experimentally derived associations between offspring size and metrics of offspring fitness. The present study also contributes to a growing literature which suggests that the fitness consequences of egg size variation are often more pronounced during the early juvenile stage, as opposed to the egg or larval stage.

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
Fig. 3

Similar content being viewed by others

References

  • Allen RM, Buckley YM, Marshall DJ (2008) Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. Am Nat 171:225–237

    Article  PubMed  Google Scholar 

  • Anibas C, Fleckenstein JH, Volze N, Buis K, Verhoeven R, Meire P, Batelaan O (2009) Transient or steady–state? Using vertical temperature profiles to quantify groundwater–surface water exchange. Hydrol Process 23(Special Issue):2165–2177

    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 Ninat River, British Columbia. Can J Fish Aquat Sci 42:1755–1765

    Article  Google Scholar 

  • Beacham TD, Murray CB (1990) Temperature, egg size, and development of embryos and alevins of five species of Pacific salmon: a comparative analysis. Trans Am Fish Soc 119:927–941

    Article  Google Scholar 

  • Beckerman AP, Benton TG, Lapsley CT, Koesters N (2006) How effective are maternal effects at having effects? Proc R Soc Lond B 273:485–493

    Article  Google Scholar 

  • Bernardo J (1996) The particular maternal effects of propagule size, especially egg size: patterns, models, quality of evidence and interpretation. Am Zool 36:216–236

    Google Scholar 

  • Bowden RM, Harms HK, Paitz RT, Janzen FJ (2004) Does optimal egg size vary with demographic stage because of physiological constraint? Funct Ecol 18:522–529

    Article  Google Scholar 

  • Brown GP, Shine R (2009) Beyond size–number trade–offs: clutch size as a maternal effect. Philol Trans R Soc Lond B 364:1097–1106

    Article  Google Scholar 

  • Carriere Y, Roff DA (1995) The evolution of offspring size and number: a test of the Smith–Fretwell model in three species of crickets. Oecologia 102:389–396

    Article  Google Scholar 

  • Congdon JD, Gibbons JW (1987) Morphological constraint on egg size: a challenge to optimal egg size theory? Proc Natl Acad Sci USA 84:4145–4147

    Article  PubMed  CAS  Google Scholar 

  • Creighton JC (2005) Population density, body size and phenotypic plasticity of brood size in a burying beetle. Behav Ecol 16:1031–1036

    Article  Google Scholar 

  • Crisp DT, Carling PA (1989) Observations on sitting, dimensions and structure of salmonid redds. J Fish Biol 34:119–134

    Article  Google Scholar 

  • Devries P (1997) Riverine salmonid egg burial depths: review of published data and implications for scour studies. Can J Fish Aquat Sci 54:1685–1698

    Google Scholar 

  • Dias GM, Marshall DJ (2010) Does the relationship between offspring size and performance change across the life-history? Oikos 119:154–162

    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 Lond B 266:2095–2100

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Einum S, Fleming IA (2000b) Highly fecund mothers sacrifice offspring survival to maximise fitness. Nature 405:565–567

    Article  PubMed  CAS  Google Scholar 

  • Einum S, Fleming IA (2002) Does within-population variation in fish egg size reflect maternal influences on optimal values? Am Nat 160:756–765

    Article  PubMed  Google Scholar 

  • Einum S, Nislow KH (2005) Local-scale density-dependent survival of mobile organisms in continuous habitats: an experimental test using Atlantic salmon. Oecologia 143:203–210

    Article  PubMed  Google Scholar 

  • Einum S, Hendry AP, Fleming IA (2002) Egg-size evolution in aquatic environments: does oxygen availability constrain size? Proc R Soc Lond B 269:2325–2330

    Article  Google Scholar 

  • Einum S, Nislow KH, McKelvey S, Armstrong JD (2008) Nest distribution shaping within-stream variation in Atlantic salmon juvenile abundance and competition over small spatial scales. J Anim Ecol 77:167–172

    Article  PubMed  Google Scholar 

  • Fischer B, Taborsky B, Kokko H (2011) How to balance the offspring quality–quantity trade off when environmental cues are unreliable. Oikos 120:258–270

    Article  Google Scholar 

  • Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fish 6:379–416

    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 

  • Fox CW, Thakar MS, Mousseau TA (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat 149:149–163

    Article  Google Scholar 

  • Fukushima M, Quinn TJ, Smoker WW (1998) Estimation of eggs lost from superimposed pink salmon (Oncorhynchus gorbuscha) redds. Can J Fish Aquat Sci 55:618–625

    Article  Google Scholar 

  • Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136

    Article  PubMed  CAS  Google Scholar 

  • Gillooli JF, Charnov EL, West GB, Savage VM, Brown JH (2001) Effects of size and temperature on development time. Nature 417:70–73

    Article  Google Scholar 

  • Gould SJ, Lewontin RC (1979) The spandrels of San Marco and the panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B 205:581–598

    Article  PubMed  CAS  Google Scholar 

  • Hannah DM, Malcolm IA, Soulsby C, Youngson AF (2004) Heat exchanges and temperatures within a salmon spawning stream in the cairngorms, Scotland: seasonal and sub-seasonal dynamics. River Res Appl 20:635–652

    Article  Google Scholar 

  • Hayes JW (1987) Competition for spawning space between brown (Salmo trutta) and rainbow trout (S. gairdneri) in a lake inlet tributary, New Zealand. Can J Fish Aquat Sci 44:40–47

    Article  Google Scholar 

  • Hendriks AJ, Mulder C (2008) Scaling of offspring number and mass to plant and animal size: model and meta-analysis. Oecologia 155:705–716

    Article  PubMed  Google Scholar 

  • Hendry AP, Day T (2003) Revisiting the positive correlation between female size and egg size. Evol Ecol Res 5:421–429

    Google Scholar 

  • Hendry AP, Day T, Cooper AB (2001) Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness. Am Nat 157:387–407

    Article  PubMed  CAS  Google Scholar 

  • Houde ALS, Fraser DJ, O’Reilly, Hutchings JA (2011) Maternal and paternal effects on fitness correlates in outbred and inbred Atlantic salmon, Salmo salar. Can J Fish Aquat Sci (in press)

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

    Article  Google Scholar 

  • Ingendahl D (2001) Dissolved oxygen concentration and emergence of sea trout fry from natural redds in tributaries of the River Rhine. J Fish Biol 58:325–341

    Article  Google Scholar 

  • Jakobsson A, Eriksson O (2000) A comparative study of seed number, seed size, seedling size and recruitment in grassland plants. Oikos 88:494–502

    Article  Google Scholar 

  • Kindsvater HK, Alonzo SH, Mangel M, Bonsall MB (2010) Effects of age- and state-dependent allocation on offspring size and number. Evol Ecol Res 12:327–346

    Google Scholar 

  • Kondolf GM, Wolman MG (1993) The sizes of salmonid spawning gravels. Water Resour Res 29:2275–2285

    Article  Google Scholar 

  • Lalonde RG (2005) Egg size variation does not increase offspring performance under interspecific competition in Nasonia vitripennis, a gregarious parasitoid. J Anim Ecol 74:630–635

    Article  Google Scholar 

  • Leips J, Richardson JML, Rodd HF, Travis J (2009) Adaptive maternal adjustments of offspring size in response to conspecific density in two populations of the least killfish, Heterandria Formosa. Evolution 63:1341–1347

    Article  PubMed  Google Scholar 

  • Malcolm IA, Soulsby C, Youngson AF, Hannah DM, McLaren IS, Thorne A (2004) Hydrological influences on hyporheic water quality: implications for salmon egg survival. Hydrol Process 181:543–1560

    Google Scholar 

  • Marshall DJ, Keough MJ (2008) The relationship between offspring size and performance in the sea. Am Nat 171:214–224

    Article  PubMed  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • Marshall DJ, Bonduriansky R, Bussiere LF (2008) Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 89:2506–2517

    Article  PubMed  Google Scholar 

  • Marshall DJ, Heppell S, Munch S, Warner R (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 

  • McGinley MA (1989) The influence of a positive correlation between clutch size and offspring fitness on the optimal egg size. Evol Ecol 3:150–156

    Article  Google Scholar 

  • McGinley MA, Temme DH, Geber MA (1987) Parental investment in offspring in variable environments: theoretical and empirical considerations. Am Nat 130:370–398

    Article  Google Scholar 

  • Michaud J, Taggart CT (2007) Lipid and gross energy content of North Atlantic right whale food, Calanus finmarchicus, in the Bay of Fundy. Endanger Species Res 3:77–94

    Article  Google Scholar 

  • Montgomery DR, Buffington JM, Peterson NP, Schette–Hames D, Quinn TP (1996) Stream-bed scour, egg burial depths, and the influence of salmonid spawning on bed surface mobility and embryo survival. Can J Fish Aquat Sci 53:1061–1070

    Article  Google Scholar 

  • Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592

    Article  Google Scholar 

  • Peterson NP, Quinn TP (1996) Spatial and temporal variation in dissolved oxygen in natural egg pockets of chum salmon, in Kennedy Creek, Washington. J Fish Biol 48:131–143

    Article  Google Scholar 

  • Plaistow SJ, St Clair JJH, Grant J, Benton TG (2007) How to put all your eggs in one basket: empirical patterns of offspring provisioning throughout a mother’s lifetime. Am Nat 170:520–529

    Article  PubMed  Google Scholar 

  • Quinn TP, Hendry AP, Wetzel LA (1995) The influence of life history trade-offs and the size of incubation gravels on egg size variation in sockeye salmon (Oncorhynchus nerka). Oikos 74:425–438

    Article  Google Scholar 

  • Rennie CD, Miller RG (2000) Spatial variability of streambed scour and fill: a comparison of scour depth in chum salmon (Oncorhynchus keta) redds and adjacent bed. Can J Fish Aquat Sci 57:928–938

    Article  Google Scholar 

  • Resetarits WJ Jr (1996) Oviposition site choice and life history evolution. Am Zool 36:205–215

    Google Scholar 

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

    Google Scholar 

  • Rollinson N, Brooks RJ (2008) Optimal offspring provisioning when egg size is “constrained”: a case study with the painted turtle Chrysemys picta. Oikos 117:144–151

    Article  Google Scholar 

  • Rollinson N, Hutchings JA (2011) Why does egg size increase with maternal size? Effects of egg size and egg density on offspring phenotypes in Atlantic salmon (Salmo salar). Evol Ecol Res (in press)

  • Rombough PJ (1985) Initial egg weight, time to maximum alevin wet weight, and optimal ponding times for Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 42:287–291

    Article  Google Scholar 

  • Rombough PJ (2006) Oxygen as a constraining factor in egg size evolution in salmonids. Can J Fish Aquat Sci 64:692–699

    Article  Google Scholar 

  • Sakai S, Harada Y (2001) Why do large mothers produce large offspring? A theory and a test. Am Nat 157:348–359

    Article  PubMed  CAS  Google Scholar 

  • Sato T, Suzuki N (2010) Female size as a determinant of larval size, weight and survival period in the coconut crab, Birgus latro. J Crustacean Biol 30:624–628

    Article  Google Scholar 

  • Sinervo B, Doughty P, Huey RB, Zamudio K (1992) Allometric engineering: a causal analysis of natural selection on offspring size. Science 248:1927–1930

    Article  Google Scholar 

  • Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108:499–506

    Article  Google Scholar 

  • Staub NL, De Beer M (1997) The role of androgens in female vertebrates. Gen Comp Endocrinol 108:1–24

    Article  PubMed  CAS  Google Scholar 

  • Steen RP, Quinn TP (1999) Egg burial depth by sockeye (Oncorhynchus nerka): implications for survival of embryos and natural selection on female body size. Can J Zool 77:836–841

    Google Scholar 

  • Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleosts. Rev Fish Biol Fish 6:287–318

    Article  Google Scholar 

  • van den Berghe EP, Gross M (1989) Natural selection resulting from female breeding competition in a pacific salmon (Coho: Oncorhychus kisutch). Evolution 43:125–140

    Article  Google Scholar 

  • White HC (1942) Atlantic salmon redds and artificial spawning beds. J Fish Res Board Can 6:37–44

    Article  Google Scholar 

Download references

Acknowledgments

We thank M. Yates, S. Mogensen, D. Keith, P. Debes, J. Porter, A.L. Houde and J. Eddington for laboratory assistance, as well as three anonymous reviewers for their critical comments. Research was also supported by Beth Lenentine and the Department of Fisheries and Oceans. Animal use was approved by the Dalhousie University Committee on Laboratory Animals. Research was funded by a Natural Sciences and Engineering Research Council Discovery grant to J.A. Hutchings, and by an Alexander Graham Bell Natural Sciences and Engineering Council grant to N. Rollinson.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Njal Rollinson.

Additional information

Communicated by Marc Mangel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rollinson, N., Hutchings, J.A. Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon. Oecologia 166, 889–898 (2011). https://doi.org/10.1007/s00442-011-1945-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-1945-9

Keywords

Navigation