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Are yolk androgens and carotenoids in barn swallow eggs related to parental quality?

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Abstract

Recently, evidence is mounting that females can adaptively engineer the quality of their offspring via the deposition of yolk compounds, including carotenoids and androgens. In this study, we simultaneously consider how both carotenoids and androgens in egg yolk relate to parental quality in barn swallows (Hirundo rustica erythrogaster). First, we found no relationship between concentrations or amounts of yolk androgens and carotenoids. Yolk carotenoids decreased with laying order, whereas we found no relationship between yolk androgens and laying order. Second, we tested the Investment Hypothesis, which predicts that high-quality females or females paired to high quality mates, allocate differentially more of these yolk compounds to their offspring. For carotenoids, we mostly found evidence to counter predictions of the Investment hypothesis: (1) Carotenoid concentrations varied among females, (2) heavier eggs contained lower carotenoid concentrations, although heavier yolks contained greater amounts of carotenoids, (3) eggs of earlier-laying females had lower concentrations in their eggs, and (4) yolk carotenoids were not correlated with clutch size or male plumage ornamentation. For androgens, we found weak support for the Investment Hypothesis: (1) Yolk androgens varied among females, (2) heavier eggs and yolks contained greater amounts, although not concentrations of androgens, (3) females paired to more colorful males laid eggs with greater concentrations of androgens, and (4) no effects of laying date or morphological correlates of female quality on androgen concentrations in egg yolks. Overall, these findings suggest that each yolk compound may have different functions and therefore may be regulated by different mechanisms.

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References

  • Ardia DR (2005) Individual quality mediates tradeoffs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524

    Article  Google Scholar 

  • Badyaev AV, Acevedo Seaman D, Navara KJ, Hill GE, Mendonca T (2006) Evolution of sex-biased maternal effects in birds. III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. J Evol Biol 19:1044–1057

    Article  PubMed  CAS  Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Moller AP, Trewby ML, Kennedy MW (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    Article  CAS  Google Scholar 

  • Bortolotti GR, Negro JJ, Surai PR, Prieto P (2003) Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol Biochem Zool 76:367–374

    Article  PubMed  CAS  Google Scholar 

  • Brown CR, Brown MB (1999) Barn swallow (Hirundo rustica). No. 42. In: Poole A, Gill F (eds) The birds of North America. The Birds of North America, Philadelphia, PA, pp 1–32

    Google Scholar 

  • Brown CR, Sherman LC (1989) Variation in the appearance of swallow eggs and the detection of intraspecific brood parasitism. Condor 91:620–627

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: Energetic adjustment in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846

    Article  CAS  Google Scholar 

  • Eising CM, Muller W, Groothuis TGG (2006) Avian mothers create different phenotypes by hormone deposition in their eggs. Biol Lett 2:20–22

    Article  PubMed  Google Scholar 

  • Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128

    Article  PubMed  CAS  Google Scholar 

  • Gil D, Lebouche G, Lacroix A, Cue R, Kreutzer M (2004) Female canaries produce eggs with greater amounts of testosterone when exposed to preferred male song. Horm Behav 45:64–70

    Article  PubMed  CAS  Google Scholar 

  • Gil D, Ninni P, Lacroix A, deLope F, Tirard C, Marzal A, Møller AP (2005) Yolk androgens in the barn swallow Hirundo rustica: a test of some adaptive hypotheses. J Evol Biol 19:123–131

    Article  CAS  Google Scholar 

  • Groothius TCC, Muller W, Engelhardt NV, Carere C, Eising C (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 9:329–352

    Article  CAS  Google Scholar 

  • Groothius TCC, Eising CM, Blount JD, Surai P, Apanius V, Dijkstra C, Muller W (2006) Multiple pathways of maternal effects in black-headed gulls: constraint and adaptive compensatory adjustment. J Evol Biol 19:1304–1313

    Article  Google Scholar 

  • Gwinner H, Schwabl H (2005) Evidence for sexy sons in European starlings (Sturnis vulgaris). Behav Ecol Sociobiol 58:375–382

    Article  Google Scholar 

  • Hill GE (1998) An easy, inexpensive means to quantify plumage coloration. J Field Ornithol 69:353–363

    Google Scholar 

  • Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:S2–S25

    Article  Google Scholar 

  • Krinsky NI (2001) Carotenoids as antioxidants. Nutrition 17:815–817

    Article  PubMed  CAS  Google Scholar 

  • Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B 267:2005–2010

    Article  CAS  Google Scholar 

  • Lipar JL, Ketterson ED, Nolan V, Casto JM (1999) Egg yolk layers vary in the concentration of steroid hormones in two avian species. Gen Compar Endocrinol 115:220–227

    Article  CAS  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (2002) SAS system for mixed models. SAS Institute, Cary, NC

    Google Scholar 

  • Marshall RC, Leisler B, Catchpole CK, Schwabl H (2005) Male song quality affects circulating but not yolk steroid concentrations in female canaries (Serinus canaria). J Exp Biol 208:4593–4598

    Article  PubMed  CAS  Google Scholar 

  • McGraw KJ (2006) Carotenoids mediate a trade-off between egg quantity and quality in Japanese quail. Ethol Ecol Evol 18:247–256

    Article  Google Scholar 

  • McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712

    Article  PubMed  Google Scholar 

  • McGraw KJ, Hill GE, Stradi R, Parker RS (2002) The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch. Comp Biochem Physiol B 131(2):261–269

    Article  PubMed  CAS  Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colourful songbird. Naturwissenschaften 92:375–338

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Rueda G (2007) Yolk androgen deposition as a female tactic to manipulate paternal contribution. Behav Ecol 18:496–498

    Article  Google Scholar 

  • Müller W, Groothuis TGG, Kasprizik A, Dijkstra C, Alatalo RV, Sittari H (2005) Prenatal androgen exposure modulates cellular and immune function of black-headed gull chicks. Proc R Soc Lond B 272:1971–1977

    Article  CAS  Google Scholar 

  • Navara KJ, Hill GE, Mendonca MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78:570–578

    Article  PubMed  CAS  Google Scholar 

  • Navara KJ, Badyaev AV, Mendonca MT, Hill GE (2006) Yolk antioxidants vary with male attractiveness and female condition in the house finch (Carpodacus mexicanus). Physiol Biochem Zool 79:1098–1105

    Article  PubMed  CAS  Google Scholar 

  • Neuman CR, Safran RJ, Lovette IJ (2007) Male tail streamer length does not predict apparent or genetic reproductive success in north American barn swallows Hirundo rustica erythrogaster. J Avian Biol 38:28–36

    Article  Google Scholar 

  • Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European Staring Sturnus vulgaris. Funct Ecol 18:58–66

    Article  Google Scholar 

  • Pilz KM, Smith HG, Sandell M, Schwabl H (2003) Inter-female variation in egg yolk androgen allocation in the European starling: Do high quality females invest more? Anim Behav 65:841–850

    Article  Google Scholar 

  • Pilz KM, Quiroga M, Schwabl H, Adkins-Regan E (2004) European starling chicks benefit from high yolk testosterone levels during a drought year. Horm Behav 46:179–192

    Article  PubMed  CAS  Google Scholar 

  • Price T (1998) Maternal and paternal effects in birds: effects on offspring fitness. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 202–226

    Google Scholar 

  • Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Funct Ecol 3:298–306

    Article  Google Scholar 

  • Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385

    Article  Google Scholar 

  • Royle NJ, Surai PF, Hartley IR (2003) The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct Ecol 17:472–481

    Article  Google Scholar 

  • Rutstein AN, Gilbert L, Slater PJB, Graves JA (2005) Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav Ecol 16:62–69

    Article  Google Scholar 

  • Safran RJ (2004) Adaptive site selection rules and variation in group size of barn swallows: individual decisions predict population patterns. Am Nat 164:121–131

    Article  Google Scholar 

  • Safran RJ, McGraw KJ (2004) Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows. Behav Ecol 15:455–461

    Article  Google Scholar 

  • Safran RJ, Neuman CR, McGraw KJ, Lovette IJ (2005) Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210–2212

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Primmer CR, Ellegren H, Møller AP (1997) An experimental study of paternity and tail ornamentation in the barn swallow (Hirundo rustica). Evolution 51:562–570

    Article  Google Scholar 

  • Saino N, Bertacche V, Ferrari RP, Martinelli R, Møller AP, Stradi R (2002) Carotenoid concentration in barn swallow eggs is influenced by laying order, maternal infection, and paternal ornamentation. Proc R Soc Lond B 269:1729–1733

    Article  CAS  Google Scholar 

  • Saino N, Ferrari RP, Romano M, Martinelli R, Møller AP (2003) Experimental manipulation of egg carotenoids affects immunity in barn swallow nestlings. Proc R Soc Lond B 270:2485–2489

    Article  Google Scholar 

  • Saino N, Ferrari RP, Romano M, Martinelli R, Lacroix A, Gil D, Møller AP (2006) Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol 17:172–181

    Article  Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Nat Acad Sci 90:11446–11450

    Article  PubMed  CAS  Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Compar Biochem Physiol 114A:271–276

    Article  CAS  Google Scholar 

  • Schwabl H (1997) Maternal androgen hormones in the egg. In: Harvey S, Etches RJ (eds) Perspectives in avian endocrinology. Journal Endocrinology, Bristol, pp 3–13

    Google Scholar 

  • Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B 267:1451–1456

    Article  CAS  Google Scholar 

  • Surai PF, Speake BK, Wood NAR, Blount JD, Bortolotti GR, Sparks NHC (2001) Carotenoid discrimination by the avian embryo: a less from wild birds. Comp Biochem Physiol B 128:743–750

    Article  PubMed  CAS  Google Scholar 

  • Tanvez A, Beguin N, Chastel O, Lacroix A, Leboucher G (2004) Sexually attractive phrases increase yolk androgens deposition in Canaries (Serinus canaries). Gen Comp Endocrinol 138:113–120

    Article  PubMed  CAS  Google Scholar 

  • Van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142

    Article  Google Scholar 

  • Verboven N, Evans NP, D’alba L, Nager RG, Blount JD, Surai PF, Monaghan P (2005) Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav Ecol Sociobiol 57:357–365

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wingfield JC, Farner DS (1975) The determination of five androgens in avian plasma by radioimmunoassay and competitive protein-binding. Androgens 26:311–327

    CAS  Google Scholar 

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Acknowledgments

John Anderson and Maura Byrne were invaluable during the field portion of this study. Funding for this study was obtained by the Cornell University chapter of Sigma Xi and the American Museum of Natural History. R.J. Safran was supported by an American Association of University Women Fellowship during data collection and a Princeton University Council on Science and Technology Fellowship during manuscript preparation; K.M. Pilz was supported by a Howard Hughes Medical Institute Predoctoral Fellowship, K.J. McGraw was supported by an EPA STAR Fellowship, and S. Correa was supported by a SUNY Minority Fellowship during the data collection phase of this project. We acknowledge the insightful comments of the Hau and Wikelski Labs at Princeton University, Ian Hartley, and two anonymous reviewers whose suggestions greatly improved our manuscript. Permission to collect eggs was granted by the US Fish and Wildlife Service and the New York Department of Environmental Conservation.

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Correspondence to Rebecca J. Safran.

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Communicated by I. Hartley

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Safran, R.J., Pilz, K.M., McGraw, K.J. et al. Are yolk androgens and carotenoids in barn swallow eggs related to parental quality?. Behav Ecol Sociobiol 62, 427–438 (2008). https://doi.org/10.1007/s00265-007-0470-7

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