Oecologia

, Volume 174, Issue 3, pp 631–638 | Cite as

The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models

  • Erik Postma
  • Heli Siitari
  • Hubert Schwabl
  • Heinz Richner
  • Barbara Tschirren
Physiological ecology - Original research

Abstract

Egg components are important mediators of prenatal maternal effects in birds and other oviparous species. Because different egg components can have opposite effects on offspring phenotype, selection is expected to favour their mutual adjustment, resulting in a significant covariation between egg components within and/or among clutches. Here we tested for such correlations between maternally derived yolk immunoglobulins and yolk androgens in great tit (Parus major) eggs using a multivariate mixed-model approach. We found no association between yolk immunoglobulins and yolk androgens within clutches, indicating that within clutches the two egg components are deposited independently. Across clutches, however, there was a significant negative relationship between yolk immunoglobulins and yolk androgens, suggesting that selection has co-adjusted their deposition. Furthermore, an experimental manipulation of ectoparasite load affected patterns of covariance among egg components. Yolk immunoglobulins are known to play an important role in nestling immune defence shortly after hatching, whereas yolk androgens, although having growth-enhancing effects under many environmental conditions, can be immunosuppressive. We therefore speculate that variation in the risk of parasitism may play an important role in shaping optimal egg composition and may lead to the observed pattern of yolk immunoglobulin and yolk androgen deposition across clutches. More generally, our case study exemplifies how multivariate mixed-model methodology presents a flexible tool to not only quantify, but also test patterns of (co)variation across different organisational levels and environments, allowing for powerful hypothesis testing in ecophysiology.

Keywords

Maternal antibodies Yolk testosterone Egg composition Parasites Maternal effects 

References

  1. Rubolini D et al (2011) Maternal effects mediated by egg quality in the yellow-legged gull Larus michahellis in relation to laying order and embryo sex. Front Zool 8:24 doi:10.1186/1742-9994-1188-1124
  2. Boonekamp JJ, Ros AHF, Verhulst S (2008) Immune activation suppresses plasma testosterone level: a meta-analysis. Biol Lett 4:741–744PubMedCentralPubMedCrossRefGoogle Scholar
  3. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23:282–288PubMedCrossRefGoogle Scholar
  4. Buechler K, Fitze PS, Gottstein B, Jacot A, Richner H (2002) Parasite-induced maternal response in a natural bird population. J Anim Ecol 71:247–252CrossRefGoogle Scholar
  5. Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. The University of Chicago Press, Chicago, pp 67–100Google Scholar
  6. Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26PubMedCrossRefGoogle Scholar
  7. Curno O, Behnke JM, McElligott AG, Reader T, Barnard CJ (2009) Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy. Proc R Soc B 276:1047–1054PubMedCrossRefGoogle Scholar
  8. Ewen JG, Thorogood R, Brekke P, Cassey P, Karadas F, Armstrong DP (2009) Maternally invested carotenoids compensate costly ectoparasitism in the hihi. Proc Natl Acad Sci USA 106:12798–12802PubMedCrossRefGoogle Scholar
  9. Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc R Soc B 268:647–650PubMedCrossRefGoogle Scholar
  10. Gasparini J, McCoy KD, Staszewski V, Haussy C, Boulinier T (2006) Dynamics of anti-Borrelia antibodies in blacklegged kittiwake (Rissa tridactyla) chicks suggest a maternal educational effect. Can J Zool 84:623–627CrossRefGoogle Scholar
  11. Gasparini J, Boulinier T, Gill VA, Gil D, Hatch SA, Roulin A (2007) Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird. J Evol Biol 20:874–880PubMedCrossRefGoogle Scholar
  12. Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. In: Brockmann HJ, Roper TJ, Naguib M, Wynne-Edwards KE, Barnard C, Mitani J (eds) Advances in the study of behavior, vol 38. Elsevier, Amsterdam, pp 337–398Google Scholar
  13. Gil D, Marzal A, de Lope F, Puerta M, Moller AP (2006) Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system. Behav Ecol Sociobiol 60:96–100CrossRefGoogle Scholar
  14. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml: user guide Release 3.0. VSN International, Hemel Hempstead, UKGoogle Scholar
  15. Grindstaff JL (2008) Maternal antibodies reduce costs of an immune response during development. J Exp Biol 211:654–660PubMedCrossRefGoogle Scholar
  16. Grindstaff JL, Brodie ED III, Ketterson ED (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc B 270:2309–2319PubMedCrossRefGoogle Scholar
  17. Grindstaff JL, Hasselquist D, Nilsson JA, Sandell M, Smith HG, Stjernman M (2006) Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity. Proc R Soc B 273:2551–2557PubMedCrossRefGoogle Scholar
  18. Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661PubMedCrossRefGoogle Scholar
  19. Groothuis TGG, Eising CM, Dijkstra C, Müller W (2005a) Balancing between costs and benefits of maternal hormone deposition in avian eggs. Biol Lett 1:78–81PubMedCentralPubMedCrossRefGoogle Scholar
  20. Groothuis TGG, Müller W, von Engelhardt N, Carere C, Eising C (2005b) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352PubMedCrossRefGoogle Scholar
  21. Groothuis TGG et al (2006) Multiple pathways of maternal effects in black-headed gull eggs: constraint and adaptive compensatory adjustment. J Evol Biol 19:1304–1313PubMedCrossRefGoogle Scholar
  22. Hargitai R, Matus Z, Hegyi G, Michl G, Toth G, Török J (2006) Antioxidants in the egg yolk of a wild passerine: differences between breeding seasons. Comp Biochem Physiol B 143:145–152PubMedCrossRefGoogle Scholar
  23. Hargitai R, Arnold KE, Herényi M, Prechl J, Török J (2009) Egg composition in relation to social environment and maternal physiological condition in the collared flycatcher. Behav Ecol Sociobiol 63:869–882CrossRefGoogle Scholar
  24. Hasselquist D, Nilsson JA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil Trans R Soc B 364:51–60PubMedCrossRefGoogle Scholar
  25. Heeb P, Werner I, Kölliker M, Richner H (1998) Benefits of induced host responses against an ectoparasite. Proc R Soc B 265:51–56CrossRefGoogle Scholar
  26. Heylen D, Muller W, Groothuis TGG, Matthysen E (2012) Female great tits do not alter their yolk androgen deposition when infested with a low-transmittable ectoparasite. Behav Ecol Sociobiol 66:287–293CrossRefGoogle Scholar
  27. Hirota Y, Suzuki T, Chazono Y, Bito Y (1976) Humoral immune responses characteristic of testosterone propionate treated chickens. Immunology 30:341–348PubMedGoogle Scholar
  28. Jacquin L, Blottiere L, Haussy C, Perret S, Gasparini J (2012) Prenatal and postnatal parental effects on immunity and growth in ‘lactating’ pigeons. Funct Ecol 26:866–875CrossRefGoogle Scholar
  29. Kankova Z, Zeman M, Okuliarova M (2012) Growth and innate immunity are not limited by selection for high egg testosterone content in Japanese quail. J Exp Biol 215:617–622PubMedCrossRefGoogle Scholar
  30. King MO, Owen JP, Schwabl H (2011) Injecting the mite into ecological immunology: measuring the antibody response of house sparrows (Passer domesticus) challenged with hematophagous mites. Auk 128:340–345CrossRefGoogle Scholar
  31. Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43:485–503CrossRefGoogle Scholar
  32. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc B 363:1635–1645PubMedCrossRefGoogle Scholar
  33. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar
  34. Müller W, Groothuis TGG, Kasprzik A, Dijkstra C, Alatalo RV, Siitari H (2005) Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proc R Soc B 272:1971–1977PubMedCrossRefGoogle Scholar
  35. Navara KJ, Hill GE, Mendonca MT (2005) Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol Biochem Zool 78:570–578PubMedCrossRefGoogle Scholar
  36. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New YorkCrossRefGoogle Scholar
  37. Postma E, Charmantier A (2007) What ‘animal models’ can and cannot tell ornithologists about the genetics of wild populations. J Ornithol 148:S633–S642CrossRefGoogle Scholar
  38. Postma E, Spyrou N, Rollins LA, Brooks RC (2011) Sex-dependent selection differentially shapes genetic variation on and off the guppy Y chromosome. Evolution 65:2145–2156PubMedCrossRefGoogle Scholar
  39. Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21:408–421CrossRefGoogle Scholar
  40. Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62:703–710CrossRefGoogle Scholar
  41. Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385CrossRefGoogle Scholar
  42. Schroderus E et al (2010) Intra- and intersexual trade-offs between testosterone and immune system: implications for sexual and sexually antagonistic selection. Am Nat 176:E90–E97PubMedCrossRefGoogle Scholar
  43. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450PubMedCrossRefGoogle Scholar
  44. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  45. Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93:241–248PubMedCrossRefGoogle Scholar
  46. Staszewski V, Reece SE, O’Donnell AJ, Cunningham EJA (2012) Drug treatment of malaria infections can reduce levels of protection transferred to offspring via maternal immunity. Proc R Soc B 279:2487–2496PubMedCrossRefGoogle Scholar
  47. Tripet F, Richner H (1997) The coevolutionary potential of a ‘generalist’ parasite, the hen flea Ceratophyllus gallinae. Parasitology 115:419–427PubMedCrossRefGoogle Scholar
  48. Tripet F, Jacot A, Richner H (2002) Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 83:935–945CrossRefGoogle Scholar
  49. Tschirren B, Richner H, Schwabl H (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc B 271:1371–1375PubMedCrossRefGoogle Scholar
  50. Tschirren B, Saladin V, Fitze PS, Schwabl H, Richner H (2005) Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings. J Anim Ecol 74:675–682CrossRefGoogle Scholar
  51. Tschirren B, Sendecka J, Groothuis TGG, Gustafsson L, Doligez B (2009a) Heritable variation in maternal yolk hormone transfer in a wild bird population. Am Nat 174:557–564PubMedCrossRefGoogle Scholar
  52. Tschirren B, Siitari H, Saladin V, Richner H (2009b) Transgenerational immunity in a bird-ectoparasite system: do maternally transferred antibodies affect parasite fecundity or the offspring’s susceptibility to fleas? Ibis 151:160–170CrossRefGoogle Scholar
  53. Wilson AJ, et al. (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26PubMedCrossRefGoogle Scholar
  54. Wolf JB, Brodie ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Erik Postma
    • 1
  • Heli Siitari
    • 2
  • Hubert Schwabl
    • 3
  • Heinz Richner
    • 4
  • Barbara Tschirren
    • 1
  1. 1.Institute of Evolutionary Biology and Environmental StudiesUniversity of ZurichZurichSwitzerland
  2. 2.Department of Biological and Environmental ScienceUniversity of JyväskyläJyväskyläFinland
  3. 3.Centre for Reproductive Biology, School of Biological SciencesWashington State UniversityPullmanUSA
  4. 4.Institute of Ecology and EvolutionUniversity of BernBernSwitzerland

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