Eggshell spottiness reflects maternally transferred antibodies in blue tits

PLoS One. 2012;7(11):e50389. doi: 10.1371/journal.pone.0050389. Epub 2012 Nov 30.

Abstract

Blue-green and brown-spotted eggshells in birds have been proposed as sexual signals of female physiological condition and egg quality, reflecting maternal investment in the egg. Testing this hypothesis requires linking eggshell coloration to egg content, which is lacking for brown protoporphyrin-based pigmentation. As protoporphyrins can induce oxidative stress, and a large amount in eggshells should indicate either high female and egg quality if it reflects the female's high oxidative tolerance, or conversely poor quality if it reflects female physiological stress. Different studies supported either predictions but are difficult to compare given the methodological differences in eggshell-spottiness measurements. Using the blue tit Cyanistes caeruleus as a model species, we aimed at disentangling both predictions in testing if brown-spotted eggshell could reflect the quality of maternal investment in antibodies and carotenoids in the egg, and at improving between-study comparisons in correlating several common measurements of eggshell coloration (spectral and digital measures, spotted surface, pigmentation indices). We found that these color variables were weakly correlated highlighting the need for comparable quantitative measurements between studies and for multivariate regressions incorporating several eggshell-color characteristics. When evaluating the potential signaling function of brown-spotted eggshells, we thus searched for the brown eggshell-color variables that best predicted the maternal transfer of antibodies and carotenoids to egg yolks. We also tested the effects of several parental traits and breeding parameters potentially affecting this transfer. While eggshell coloration did not relate to yolk carotenoids, the eggs with larger and less evenly-distributed spots had higher antibody concentrations, suggesting that both the quantity and distribution of brown pigments reflected the transfer of maternal immune compounds in egg yolks. As yolk antibody concentrations were also positively related to key proxies of maternal quality (egg volume, number, yellow feather brightness, tarsus length), eggshells with larger spots concentrated at their broad pole may indicate higher-quality eggs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies / analysis*
  • Antibodies / immunology
  • Carotenoids / analysis
  • Carotenoids / chemistry
  • Color
  • Egg Shell / anatomy & histology
  • Egg Shell / chemistry*
  • Egg Yolk / chemistry*
  • Egg Yolk / immunology
  • Female
  • Ovum / chemistry*
  • Ovum / immunology
  • Passeriformes / physiology*
  • Pigmentation / physiology*
  • Protoporphyrins / analysis
  • Protoporphyrins / chemistry

Substances

  • Antibodies
  • Protoporphyrins
  • Carotenoids

Grants and funding

This research was funded by grants of the French National Agency for Research, ANR-JC05-43762 to TB and ANR-09-JCJC-0050-01 to CD, and grants of the University of Montpellier II and the Association for the Study of Animal Behaviour ASAB to MJH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.