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Front Zool. 2018 Jun 19;15:25. doi: 10.1186/s12983-018-0272-y. eCollection 2018.

The effect of pre-laying maternal immunization on offspring growth and immunity differs across experimentally altered postnatal rearing conditions in a wild songbird.

Frontiers in zoology

Rafał Martyka, Ewa B Śliwińska, Mirosław Martyka, Mariusz Cichoń, Piotr Tryjanowski

Affiliations

  1. 1Institute of Nature Conservation, Polish Academy of Sciences, Mickiewicza 33, 31-120 Kraków, Poland.
  2. 2Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Kraków, Poland.
  3. 3Institute of Zoology, Pozna? University of Life Sciences, Wojska Polskiego 71C, 60-625 Pozna?, Poland.

PMID: 29946341 PMCID: PMC6006776 DOI: 10.1186/s12983-018-0272-y

Abstract

BACKGROUND: Prenatal antibody transfer is an immune-mediated maternal effect by which females can shape postnatal offspring resistance to pathogens and parasites. Maternal antibodies passed on to offspring provide primary protection to neonates against diverse pathogenic antigens, but they may also affect offspring growth and influence the development of an offspring's own immune response. The effects of maternal antibodies on offspring performance commonly require that the disease environment experienced by a mother prior to breeding matches the environment encountered by her offspring after hatching/birth. However, other circumstances, like postnatal rearing conditions that affect offspring food availability, may also determine the effects of maternal antibodies on offspring growth and immunity. To date, knowledge about how prenatal immune-mediated maternal effects interact with various postnatal rearing conditions to affect offspring development and phenotype in wild bird population remains elusive. Here we experimentally studied the interactive effects of pre-laying maternal immunization with a bacterial antigen (lipopolysaccharide) and post-hatching rearing conditions, altered by brood size manipulation, on offspring growth and humoral immunity of wild great tits (

RESULTS: We found that maternal immunization and brood size manipulation interactively affected the growth and specific humoral immune response of avian offspring. Among nestlings reared in enlarged broods, only those that originated from immunized mothers grew better and were heavier at fledging stage compared to those that originated from non-immunized mothers. In contrast, no such effects were observed among nestlings reared in non-manipulated (control) broods. Moreover, offspring of immunized females had a stronger humoral immune response to lipopolysaccharide during postnatal development than offspring of non-immunized females, but only when the nestling was reared in control broods.

CONCLUSIONS: This study demonstrates that offspring development and their ability to cope with pathogens after hatching are driven by mutual influences of pathogen-induced prenatal maternal effects and post-hatching rearing conditions. Our findings suggest that immune-mediated maternal effects may have context-dependent influences on offspring growth and immune function, related to the postnatal environmental conditions experienced by the progeny.

Keywords: Brood size manipulation; Food availability; Great tit; Humoral immune response; LPS; Maternal antibodies; Parus major; Prenatal maternal effects

Conflict of interest statement

The experiment and all procedures conducted on birds in the study were approved by the Poznań Local Ethics Committee for Animal Experimentation (permit number: 72/2012) and with permission from the Re

References

  1. Oecologia. 1999 Nov;121(3):316-322 - PubMed
  2. Biol Lett. 2006 Dec 22;2(4):573-6 - PubMed
  3. Mol Ecol. 1998 Aug;7(8):1071-5 - PubMed
  4. Trends Ecol Evol. 1999 Sep;14(9):343-348 - PubMed
  5. Comp Biochem Physiol C Toxicol Pharmacol. 2001 Feb;128(2):255-63 - PubMed
  6. J Exp Biol. 2008 Mar;211(Pt 5):654-60 - PubMed
  7. Proc Biol Sci. 2012 Jul 22;279(1739):2891-8 - PubMed
  8. Proc Biol Sci. 2006 Oct 7;273(1600):2551-7 - PubMed
  9. J Exp Biol. 2009 Mar;212(Pt 6):815-22 - PubMed
  10. Behav Ecol Sociobiol. 2013;67:1809-1815 - PubMed
  11. Am Nat. 2015 Jun;185(6):769-83 - PubMed
  12. Avian Pathol. 1990 Apr;19(2):345-54 - PubMed
  13. J Anim Ecol. 2006 Sep;75(5):1154-64 - PubMed
  14. Physiol Biochem Zool. 2014 Sep-Oct;87(5):740-51 - PubMed
  15. J Anim Ecol. 2007 Nov;76(6):1215-23 - PubMed
  16. Proc Biol Sci. 2014 Oct 7;281(1792):null - PubMed
  17. Proc Biol Sci. 2004 Feb 7;271 Suppl 3:S110-3 - PubMed
  18. Proc Biol Sci. 2004 Jul 7;271(1546):1371-5 - PubMed
  19. PLoS One. 2010 Mar 11;5(3):e9639 - PubMed
  20. Horm Behav. 2016 Jul;83:6-13 - PubMed
  21. Trends Ecol Evol. 2008 May;23(5):282-8 - PubMed
  22. Proc Biol Sci. 2003 Feb 7;270(1512):241-8 - PubMed
  23. Scand J Immunol. 1999 Oct;50(4):348-54 - PubMed
  24. Oecologia. 2003 Jun;136(1):148-54 - PubMed
  25. Proc Biol Sci. 2006 Jul 22;273(1595):1759-64 - PubMed
  26. Poult Sci. 1996 Mar;75(3):342-5 - PubMed
  27. Horm Behav. 2012 Aug;62(3):337-44 - PubMed
  28. Proc Biol Sci. 2003 Nov 22;270(1531):2309-19 - PubMed
  29. Philos Trans R Soc Lond B Biol Sci. 2008 May 12;363(1497):1635-45 - PubMed
  30. Biol Reprod. 1994 Dec;51(6):1173-80 - PubMed

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