Skip to main content

Advertisement

SpringerLink
Log in

Birds from matched developmental environments breed faster

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The developmental environment an animal experiences can have a pervasive and sustained effect on phenotype throughout its life. Animals exposed to suboptimal conditions during development can experience physiological trade-offs, leading to seemingly negative phenotypic changes in later life that have been hypothesised to have detrimental effects on fitness. However, few studies have investigated how exposure to suboptimal developmental conditions affects an animal’s reproductive behavior and fitness. Here, we determine if elevated levels of corticosterone (CORT; the dominant avian stress hormone) during development affect fitness via changes in reproductive investment in adult zebra finches (Taeniopygia guttata). To do this, we exposed nestling zebra finches to either CORT supplemented or control treatments and assessed their mate selection and reproductive investment as adults, using free choice breeding experiments. We found that breeding pairs of birds from matched developmental treatments (CORT or control) had a shorter latency to lay clutches compared to pairs with mismatched developmental treatments. We found no indication that clutch size or egg mass were affected by developmental treatment. Also, we found no evidence that birds choose mates to match their own developmental treatment. Our results demonstrate that developmental experience may affect reproductive investment through changes to reproductive timing and add to the literature suggesting that pairs with similar developmental backgrounds can coordinate their reproduction more effectively.

Significance statement

Developmental stress may reduce the fitness of a breeding pair as a result of its detrimental effect on phenotype and performance. Alternatively, individuals could use indicators of developmental stress to influence mate choice in order to compensate for a poor start to life. Previous studies suggest that birds do assortatively mate by developmental environment, but this has not been tested in a free choice mating context. Using a free choice breeding experiment, we show that pairs of breeding birds lay eggs faster when they have matching developmental environments, regardless of the quality of their developmental environment. This evidence suggests that assortatively mated pairs can potentially offset a bad start to life and maintain fitness in spite of the deleterious effects of developmental stress.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Data availability

The datasets generated and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Adkins-Regan E, Tomaszycki M (2007) Monogamy on the fast track. Biol Lett 3:617–619

    PubMed  PubMed Central  Google Scholar 

  • Alonso-Alvarez C, Bertrand S, Faivre B, Sorci G (2007) Increased susceptibility to oxidative damage as a cost of accelerated somatic growth in zebra finches. Funct Ecol 21:873–879

    Google Scholar 

  • Both C, Dingemanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667–674

    Google Scholar 

  • Buchanan KL, Leitner S, Spencer KA, Goldsmith AR, Catchpole CK (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc R Soc Lond B 271:2381–2386

    Google Scholar 

  • Buchanan KL, Spencer KA, Goldsmith A, Catchpole C (2003) Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc R Soc Lond B 270:1149–1156

    CAS  Google Scholar 

  • Chin EH, Love OP, Verspoor JJ, Williams TD, Rowley K, Burness G (2009) Juveniles exposed to embryonic corticosterone have enhanced flight performance. Proc R Soc Lond B 276:499–505

    Google Scholar 

  • Crespi EJ, Warne RW (2013) Environmental conditions experienced during the tadpole stage alter post-metamorphic glucocorticoid response to stress in an amphibian. Integr Comp Biol 53:989–1001

    CAS  PubMed  Google Scholar 

  • Crino OL, Driscoll SC, Breuner CW (2014a) Corticosterone exposure during development has sustained but not lifelong effects on body size and total and free corticosterone responses in the zebra finch. Gen Comp Endocr 196:123–129

    CAS  PubMed  Google Scholar 

  • Crino OL, Prather CT, Driscoll SC, Good JM, Breuner CW (2014b) Developmental stress increases reproductive success in male zebra finches. Proc R Soc B 281:20141266

    PubMed  Google Scholar 

  • Crino OL, van Oorschot BK, Crandell KE, Breuner CW, Tobalske BW (2017) Flight performance in the altricial zebra finch: developmental effects and reproductive consequences. Ecol Evol 7:2316–2326

    PubMed  PubMed Central  Google Scholar 

  • Curley JP, Mashoodh R, Champagne FA (2011) Epigenetics and the origins of paternal effects. Horm Behav 59:306–314

    PubMed  Google Scholar 

  • Erikstad KE, Asheim M, Fauchald P, Dahlhaug L, Tveraa T, Dahlhaug P (1997) Adjustment of parental effort in the puffin; the roles of adult body condition and chick size. Behav Ecol Sociobiol 40:95–100

    Google Scholar 

  • Eyck HJ, Buchanan KL, Crino OL, Jessop TS (2019) Effects of developmental stress on animal phenotype and performance: a quantitative review. Biol Rev 94:1143–1160

    PubMed  Google Scholar 

  • Fawcett TW, Johnstone RA (2003) Mate choice in the face of costly competition. Behav Ecol 14:771–779

    Google Scholar 

  • Francis D, Diorio J, Liu D, Meaney MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158

    CAS  PubMed  Google Scholar 

  • Gil D, Heim C, Bulmer E, Rocha M, Puerta M, Naguib M (2004) Negative effects of early developmental stress on yolk testosterone levels in a passerine bird. J Exp Biol 207:2215–2220

    CAS  PubMed  Google Scholar 

  • Holveck M-J, Geberzahn N, Riebel K (2011) An experimental test of condition-dependent male and female mate choice in zebra finches. PLoS One 6:e23974

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holveck M-J, Riebel K (2010) Low-quality females prefer low-quality males when choosing a mate. Proc R Soc Lond B 277:153–160

    Google Scholar 

  • Houston DC, Donnan D, Jones PJ (1995) The source of the nutrients required for egg production in zebra finches Poephila guttata. J Zool 235:469–483

    Google Scholar 

  • Houston DC, Jones PJ, Sinly RM (1983) The effect of female body condition on egg laying in lesser black-backed gulls Larus fuscus. J Zool 200:509–520

    Google Scholar 

  • Kim S-Y, Noguera JC, Morales J, Velando A (2011) Quantitative genetic evidence for trade-off between growth and resistance to oxidative stress in a wild bird. Evol Ecol 25:461–472

    Google Scholar 

  • Kjærsgaard A, Le N, Demontis D, Novičič ZK, Loeschcke V, Pertoldi C (2012) The effect of developmental temperature fluctuation on wing traits and stressed locomotor performance in Drosophila melanogaster, and its dependence on heterozygosity. Evol Ecol Res 14:803–819

    Google Scholar 

  • Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P (2011) Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev 35:1291–1301

    CAS  PubMed  Google Scholar 

  • Kraft F-LO, Driscoll SC, Buchanan KL, Crino OL (2019) Developmental stress reduces body condition across avian life-history stages: a comparison of quantitative magnetic resonance data and condition indices. Gen Comp Endocr 272:33–41

    CAS  PubMed  Google Scholar 

  • Laubu C, Dechaume-Moncharmont F-X, Motreuil S, Schweitzer C (2016) Mismatched partners that achieve postpairing behavioral similarity improve their reproductive success. Sci Adv 2:e1501013

    PubMed  PubMed Central  Google Scholar 

  • Levine S (2005) Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrino 30:939–946

    Google Scholar 

  • Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662

    CAS  PubMed  Google Scholar 

  • Loarie SR, Duffy PB, Hamilton H, Asner GP, Field CB, Ackerly DD (2009) The velocity of climate change. Nature 462:1052–1055

    CAS  PubMed  Google Scholar 

  • Mariette MM, Griffith SC (2012) Nest visit synchrony is high and correlates with reproductive success in the wild Zebra finch Taeniopygia guttata. J Avian Biol 43:131–140

    Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

    PubMed  Google Scholar 

  • Micheli-Campbell M, Campbell H, Cramp R, Booth D, Franklin C (2011) Staying cool, keeping strong: incubation temperature affects performance in a freshwater turtle. J Zool 285:266–273

    Google Scholar 

  • Møller AP, Swaddle JP (1997) Asymmetry, developmental stability and evolution. Oxford University Press, Oxford, UK

    Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc B 363:1635–1645

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Murphy MT (1986) Body size and condition, timing of breeding, and aspects of egg production in Eastern Kingbirds. Auk 103:465–476

    Google Scholar 

  • Naguib M, Nemitz A, Gil D (2006) Maternal developmental stress reduces reproductive success of female offspring in zebra finches. Proc R Soc Lond B 273:1901–1905

    Google Scholar 

  • Naguib M, Riebel K, Marzal A, Gil D (2004) Nestling immunocompetence and testosterone covary with brood size in a songbird. Proc R Soc Lond B 271:833–838

    Google Scholar 

  • Nowicki S, Peters S, Podos J (1998) Song learning, early nutrition and sexual selection in songbirds. Am Zool 38:179–190

    Google Scholar 

  • Nowicki S, Searcy W, Peters S (2002) Brain development, song learning and mate choice in birds: a review and experimental test of the “nutritional stress hypothesis”. J Comp Physiol A 188:1003–1014

    CAS  Google Scholar 

  • Rando OJ (2012) Daddy issues: paternal effects on phenotype. Cell 151:702–708

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rhees RW, Lephart ED, Eliason D (2001) Effects of maternal separation during early postnatal development on male sexual behavior and female reproductive function. Behav Brain Res 123:1–10

    CAS  PubMed  Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    PubMed  Google Scholar 

  • Roth TL, Lubin FD, Funk AJ, Sweatt JD (2009) Lasting epigenetic influence of early-life adversity on the BDNF gene. Biol Psychiatry 65:760–769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roulin A (1999) Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10:688–695

    Google Scholar 

  • Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2005) Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zool A 303:998–1006

    Google Scholar 

  • Sánchez-Macouzet O, Rodríguez C, Drummond H (2014) Better stay together: pair bond duration increases individual fitness independent of age-related variation. Proc R Soc B 281:20132843

    PubMed  Google Scholar 

  • Schoech SJ, Rensel MA, Bridge ES, Boughton RK, Wilcoxen TE (2009) Environment, glucocorticoids, and the timing of reproduction. Gen Comp Endocr 163:201–207

    CAS  PubMed  Google Scholar 

  • Schuett W, Dall SR, Royle NJ (2011) Pairs of zebra finches with similar ‘personalities’ make better parents. Anim Behav 81:609–618

    Google Scholar 

  • Schweitzer C, Schwabl H, Baran NM, Adkins-Regan E (2014) Pair disruption in female zebra finches: consequences for offspring phenotype and sensitivity to a social stressor. Anim Behav 90:195–204

    Google Scholar 

  • Scofield HN, Mattila HR (2015) Honey bee workers that are pollen stressed as larvae become poor foragers and waggle dancers as adults. PLoS One 10:e0121731

    PubMed  PubMed Central  Google Scholar 

  • Siegal ML, Bergman A (2002) Waddington's canalization revisited: developmental stability and evolution. P Natl Acad Sci USA 99:10528–10532

    CAS  Google Scholar 

  • Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139

    CAS  PubMed  Google Scholar 

  • Spencer KA, Evans NP, Monaghan P (2008) Postnatal stress in birds: a novel model of glucocorticoid programming of the hypothalamic-pituitary-adrenal axis. Endocrinology 150:1931–1934

    PubMed  Google Scholar 

  • Spencer KA, Wimpenny JH, Buchanan KL, Lovell PG, Goldsmith AR, Catchpole CK (2005) Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata). Behav Ecol Sociobiol 58:423–428

    Google Scholar 

  • Stevens DJ, Hansell MH, Freel JA, Monaghan P (1999) Developmental trade–offs in caddis flies: increased investment in larval defence alters adult resource allocation. Proc R Soc Lond B 266:1049–1054

    Google Scholar 

  • Suomi SJ (1997) Early determinants of behaviour: evidence from primate studies. Brit Med Bull 53:170–184

    CAS  PubMed  Google Scholar 

  • Vézina F, Salvante KG, Williams TD (2003) The metabolic cost of avian egg formation: possible impact of yolk precursor production? J Exp Biol 206:4443–4451

    PubMed  Google Scholar 

  • Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150:563–565

    Google Scholar 

  • Weaver IC, Meaney MJ, Szyf M (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. P Natl Acad Sci USA 103:3480–3485

    CAS  Google Scholar 

  • Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. P Natl Acad Sci USA 104:5738–5742

    CAS  Google Scholar 

  • Williams TD (2005) Mechanisms underlying the costs of egg production. Bioscience 55:39–48

    Google Scholar 

  • Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies, vol 5. Oxford University Press, Oxford

    Google Scholar 

Download references

Acknowledgments

This work was conducted with substantial help in the aviary from Anna Miltiadous. We.

also thank the Deakin Waurn Ponds Campus animal care staff, especially Dr. Rod Collins. We would like to thank two anonymous reviewers, who provided useful comments on an earlier version of the manuscript.

Funding

This work was supported by grants from Australasian Society for the Study of Animal Behaviour (ASSAB); Birdlife Australia and Australian Research Council grant number FT140100131 to KLB.

Author information

Authors and Affiliations

  1. School of Life and Environmental Sciences, Centre for Integrative Ecology, Deakin University, Geelong, Victoria, Australia

    Harrison J.F. Eyck, Ondi L. Crino, Fanny-Linn O.H. Kraft, Tim S. Jessop & Katherine L. Buchanan

  2. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia

    Harrison J.F. Eyck

Authors
  1. Harrison J.F. Eyck
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ondi L. Crino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fanny-Linn O.H. Kraft
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tim S. Jessop
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katherine L. Buchanan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Harrison J.F. Eyck.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical note

Our experiments complied with all Australian laws and were conducted under the ethics permit G15-2015, approved by Animal Ethics Committee Laboratory-Geelong (AECL-G). After the experiments concluded, birds were housed in sex-specific groups in two outdoor aviaries (3 × 1 × 2 m).

Additional information

Communicated by D. Rubenstein

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eyck, H.J., Crino, O.L., Kraft, FL.O. et al. Birds from matched developmental environments breed faster. Behav Ecol Sociobiol 74, 20 (2020). https://doi.org/10.1007/s00265-020-2798-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-020-2798-1

Keywords

Search

Navigation