The multivariate egg: quantifying within- and among-clutch correlations between maternally derived yolk immunoglobulins and yolk androgens using multivariate mixed models
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.
KeywordsMaternal antibodies Yolk testosterone Egg composition Parasites Maternal effects
- 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
- 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
- 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
- Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml: user guide Release 3.0. VSN International, Hemel Hempstead, UKGoogle Scholar
- Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar