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

Oecologia

Volumn 174, Issue 3, 2014, Pages 631-638

  Postma, Erik ^a   Siitari, Heli ^b   Schwabl, Hubert ^c   Richner, Heinz ^d   Tschirren, Barbara ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF BERN   (Switzerland)

Author keywords

Egg composition; Maternal antibodies; Maternal effects; Parasites; Yolk testosterone

Indexed keywords

ADAPTATION; ANDROGEN; BIRD; CLUTCH SIZE; CORRELATION; COVARIANCE ANALYSIS; ECOPHYSIOLOGY; ECTOPARASITE; GROWTH RESPONSE; IMMUNE RESPONSE; MULTIVARIATE ANALYSIS; OVIPARITY;

ANDROGEN; IMMUNOGLOBULIN G;

ANIMAL; ANTIGENIC VARIATION; ARTICLE; CHEMISTRY; EGG YOLK; ENVIRONMENT; FEMALE; FLEA; HOST PARASITE INTERACTION; IMMUNOLOGY; MALE; MULTIVARIATE ANALYSIS; OVIPARITY; PARASITOLOGY; PHYSIOLOGY; SONGBIRD;

ANDROGENS; ANIMALS; ANTIGENIC VARIATION; EGG YOLK; ENVIRONMENT; FEMALE; HOST-PARASITE INTERACTIONS; IMMUNOGLOBULIN G; MALE; MULTIVARIATE ANALYSIS; OVIPARITY; PASSERIFORMES; SIPHONAPTERA;

EID: 84897635786     PISSN: 00298549     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00442-013-2803-8     Document Type: Article

References (54)

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: 741-744.
3. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23: 282-288.
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: 247-252.
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 67-100.
6. Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77: 1-26.
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: 1047-1054.
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: 12798-12802.
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: 647-650.
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: 623-627.
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: 874-880.
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 337-398.
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: 96-100.
14. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml: user guide Release 3. 0. VSN International, Hemel Hempstead, UK.
15. Grindstaff JL (2008) Maternal antibodies reduce costs of an immune response during development. J Exp Biol 211: 654-660.
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: 2309-2319.
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: 2551-2557.
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: 1647-1661.
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: 78-81.
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: 329-352.
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: 1304-1313.
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: 145-152.
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: 869-882.
24. Hasselquist D, Nilsson JA (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil Trans R Soc B 364: 51-60.
25. Heeb P, Werner I, Kölliker M, Richner H (1998) Benefits of induced host responses against an ectoparasite. Proc R Soc B 265: 51-56.
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: 287-293.
27. Hirota Y, Suzuki T, Chazono Y, Bito Y (1976) Humoral immune responses characteristic of testosterone propionate treated chickens. Immunology 30: 341-348.
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: 866-875.
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: 617-622.
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: 340-345.
31. Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43: 485-503.
32. Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Phil Trans R Soc B 363: 1635-1645.
33. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New York.
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: 1971-1977.
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: 570-578.
36. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New York.
37. Postma E, Charmantier A (2007) What 'animal models' can and cannot tell ornithologists about the genetics of wild populations. J Ornithol 148: S633-S642.
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: 2145-2156.
39. Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time-scales. Funct Ecol 21: 408-421.
40. Richner H, Oppliger A, Christe P (1993) Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62: 703-710.
41. Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12: 381-385.
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-E97.
43. Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90: 11446-11450.
44. Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386: 231.
45. Sgrò CM, Hoffmann AA (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93: 241-248.
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: 2487-2496.
47. Tripet F, Richner H (1997) The coevolutionary potential of a 'generalist' parasite, the hen flea Ceratophyllus gallinae. Parasitology 115: 419-427.
48. Tripet F, Jacot A, Richner H (2002) Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 83: 935-945.
49. Tschirren B, Richner H, Schwabl H (2004) Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc B 271: 1371-1375.
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: 675-682.
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: 557-564.
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: 160-170.
53. Wilson AJ, et al. (2010) An ecologist's guide to the animal model. J Anim Ecol 79: 13-26.
54. Wolf JB, Brodie ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13: 64-69.