Interactions between prenatal maternal effects and posthatching conditions in a wild bird population

Behavioral Ecology

Volumn 25, Issue 6, 2014, Pages 1459-1466

  Giordano, Marta ^a   Groothuis, Ton G G ^b   Tschirren, Barbara ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

anticipatory maternal effects; environmental change; environmental predictability; mismatch hypothesis; prenatal maternal effects; silver spoon; yolk androgens

Indexed keywords

ADAPTATION; BIRD; ENVIRONMENTAL RESPONSE; MATERNAL CARE; MATERNAL EFFECT; PHENOTYPIC PLASTICITY; WILD POPULATION;

AVES;

EID: 84913543673     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/aru149     Document Type: Article

References (61)

1. Agrawal AA, Laforsch C, Tollrian R. 1999. Transgenerational induction of defences in animals and plants. Nature. 401: 60-63.
2. Bates D, Maechler M, Bolker B. 2011. lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42. Available from: http://CRAN.R-project.org/package=lme4.
3. Berthouly A, Helfenstein F, Richner H. 2007. Cellular immune response, stress resistance and competitiveness in nestling great tits in relation to maternally transmitted carotenoids. Funct Ecol. 21: 335-343.
4. Bolton M, Houston D, Monaghan P. 1992. Nutritional constraints on egg formation in the lesser black-backed gull: an experimental study. J Anim Ecol. 61: 521-532.
5. Both C, Visser ME, Verboven N. 1999. Density-dependent recruitment rates in great tits: the importance of being heavier. Proc R Soc Lond B. 266: 465-469.
6. Christians JK. 2002. Avian egg size: variation within species and inflexibility within individuals. Biol Rev Camb Philos Soc. 77: 1-26.
7. Cleal JK, Poore KR, Boullin JP, Khan O, Chau R, Hambidge O, Torrens C, Newman JP, Poston L, Noakes DE, et al. 2007. Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. Proc Natl Acad Sci USA. 104: 9529-9533.
8. Crean AJ, Marshall DJ. 2008. Gamete plasticity in a broadcast spawning marine invertebrate. Proc Natl Acad Sci USA. 105: 13508-13513.
9. De Witt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends Ecol Evol. 13: 77-81.
10. Fontaine JJ, Martin TE. 2006. Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett. 9: 428-434.
11. Galloway LF, Etterson JR. 2007. Transgenerational plasticity is adaptive in the wild. Science. 318: 1134-1136.
12. 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.
13. George LA, Zhang L, Tuersunjiang N, Ma Y, Long NM, Uthlaut AB, Smith DT, Nathanielsz PW, Ford SP. 2012. Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring. Am J Physiol Regul Integr Comp Physiol. 302: R795-R804.
14. Georges M, Nielsen D, Mackinnon M, Mishra A, Okimoto R, Pasquino AT, Sargeant LS, Sorensen A, Steele MR, Zhao X. 1995. Mapping quantitative trait loci controlling milk production in dairy cattle by exploiting progeny testing. Genetics. 139: 907-920.
15. Gil D, Graves J, Hazon N, Wells A. 1999. Male attractiveness and differential testosterone investment in zebra finch eggs. Science. 286: 126-128.
16. Gluckman PD, Hanson MA, Cooper C, Thornburg KL. 2008. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 359: 61-73.
17. Goodenough AE, Hart AG, Elliot SL. 2008. Variation in offspring quality with cavity orientation in the great tit. Ethol Ecol Evol. 20: 375-389.
18. Goodenough AE, Stallwood B. 2012. Differences in culturable microbial communities in bird nestboxes according to orientation and influences on offspring quality in great tits (Parus major). Microb Ecol. 63: 986-995.
19. Gorman HE, Nager RG. 2004. Prenatal developmental conditions have long-term effects on offspring fecundity. Proc R Soc Lond B. 271: 1923-1928.
20. Grafen A. 1988. On the uses of data on lifetime reproductive success. In: Clutton-Brock T, editor. Reproductive success. Chicago, IL: University of Chicago Press. p. 454-471.
21. Groothuis TG, Müller W, von Engelhardt N, Carere C, Eising C. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev. 29: 329-352.
22. Hales CN, Barker DJ. 2001. The thrifty phenotype hypothesis. Br Med Bull. 60: 5-20.
23. Hasselquist D, Nilsson JA. 2009. Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc Lond B. 364: 51-60.
24. Heeb P, Werner I, Kölliker M, Richner H. 1998. Benefits of induced host responses against an ectoparasite. Proc R Soc Lond B. 265: 51-56.
25. Helle S, Laaksonen T, Huitu O. 2013. Sex-specific offspring growth according to maternal testosterone, corticosterone, and glucose levels. Behav Ecol. 24: 205-212.
26. Henriksen R, Rettenbacher S, Groothuis TG. 2011. Prenatal stress in birds: pathways, effects, function and perspectives. Neurosci Biobehav Rev. 35: 1484-1501.
27. Hinde CA, Buchanan KL, Kilner RM. 2009. Prenatal environmental effects match offspring begging to parental provisioning. Proc R Soc Lond B. 276: 2787-2794.
28. Krist M. 2011. Egg size and offspring quality: a meta-analysis in birds. Biol Rev Camb Philos Soc. 86: 692-716.
29. Lindström J. 1999. Early development and fitness in birds and mammals. Trends Ecol Evol. 14: 343-348.
30. Lloyd JD, Martin TE. 2004. Nest-site preference and maternal effects on offspring growth. Behav Ecol. 15: 816-823.
31. Marshall DJ, Uller T. 2007. When is a maternal effect adaptive? Oikos. 116: 1957-1963.
32. Meylan S, Clobert J. 2005. Is corticosterone-mediated phenotype development adaptive? Maternal corticosterone treatment enhances survival in male lizards. Horm Behav. 48: 44-52.
33. Monaghan P. 2008. Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc Lond B. 363: 1635-1645.
34. Mousseau TA, Fox CW 1998. Maternal effects as adaptations. New York: Oxford University Press.
35. Naef-Daenzer B, Widmer F, Nuber M. 2001. Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol. 70: 730-738.
36. Nager RG, Ruegger C, van Noordwijk AJ. 1997. Nutrient or energy limitation on egg formation: a feeding experiment in great tits. J Anim Ecol. 66: 495-507.
37. Pitala N, Ruuskanen S, Laaksonen T, Doligez B, Tschirren B, Gustafsson L. 2009. The effects of experimentally manipulated yolk androgens on growth and immune function of male and female nestling collared flycatchers Ficedula albicollis. J Avian Biol. 40: 225-230.
38. Postma E, Siitari H, Schwabl H, Richner H, Tschirren B. 2014. The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models. Oecologia. 174: 631-638.
39. R Development Core Team. 2011. R: a language and environment for statistical computing [Internet]. Vienna (Austria): R Foundation for Statistical Computing [cited 2014 July 7]. Available from: http://www.Rproject.org.
40. Rickard IJ, Lummaa V. 2007. The predictive adaptive response and metabolic syndrome: challenges for the hypothesis. Trends Endocrinol Metab. 18: 94-99.
41. Romano M, Caprioli M, Ambrosini R, Rubolini D, Fasola M, Saino N. 2008. Maternal allocation strategies and differential effects of yolk carotenoids on the phenotype and viability of yellow-legged gull (Larus michahellis) chicks in relation to sex and laying order. J Evol Biol. 21: 1626-1640.
42. Russell AF, Langmore NE, Cockburn A, Astheimer LB, Kilner RM. 2007. Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science. 317: 941-944.
43. Saino N, Ferrari RP, Romano M, Martinelli R, Lacroix A, Gil D, Moller AP. 2006. Maternal allocation of androgens and antagonistic effects of yolk androgens on sons and daughters. Behav Ecol. 17: 172-181.
44. Schwabl H. 1993. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA. 90: 11446-11450.
45. Schwabl H. 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A. 114: 271-276.
46. Sheriff MJ, Love OP. 2013. Determining the adaptive potential of maternal stress. Ecol Lett. 16: 271-280.
47. Sockman KW, Schwabl H. 2000. Yolk androgens reduce offspring survival. Proc R Soc Lond B. 267: 1451-1456.
48. Thomas DW, Blondel J, Perret P, Lambrechts MM, Speakman JR. 2001. Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science. 291: 2598-2600.
49. Tinbergen JM, Boerlijst MC. 1990. Nestling weight and survival in individual great tits (Parus major). J Anim Ecol. 59: 1113-1127.
50. Tschirren B, Bischoff LL, Saladin V, Richner H. 2007a. Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Funct Ecol. 21: 372-378.
51. Tschirren B, Fitze PS, Richner H. 2003. Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol. 72: 839-845.
52. Tschirren B, Fitze PS, Richner H. 2007b. Maternal modulation of natal dispersal in a passerine bird: an adaptive strategy to cope with parasitism? Am Nat. 169: 87-93.
53. Tschirren B, Richner H. 2006. Parasites shape the optimal investment in immunity. Proc R Soc Lond B. 273: 1773-1777.
54. Tschirren B, Richner H, Schwabl H. 2004. Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proc R Soc Lond B. 271: 1371-1375.
55. 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.
56. Tschirren B, Sendecka J, Groothuis TG, Gustafsson L, Doligez B. 2009. Heritable variation in maternal yolk hormone transfer in a wild bird population. Am Nat. 174: 557-564.
57. Uller T, Nakagawa S, English S. 2013. Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol. 26: 2161-2170.
58. van der Waaij EH, van den Brand H, van Arendonk JA, Kemp B. 2011. Effect of match or mismatch of maternal-offspring nutritional environment on the development of offspring in broiler chickens. Animal. 5: 741-748.
59. van Noordwijk AJ, Cleery RH, Perrins CM. 1995. Selection for the timing of great tit breeding in relation to caterpillar growth and temperature. J Anim Ecol. 64: 451-458.
60. Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, Whitelaw C, Nager RG. 2003. Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc Lond B. 270: 2223-2232.
61. Wells JC. 2007. The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc. 82: 143-172.