Phenotypic plasticity and phenotypic stability are major components of the adaptive evolution of organisms to environmental variation. The invariant two-egg clutch size of Eudyptes penguins has recently been proposed to be a unique example of a maladaptive phenotypic stability, while their egg mass is a plastic trait. We tested whether this phenotypic plasticity during reproduction might result from constraints imposed by migration (migratory carry-over effect) and breeding (due to the depletion of female body reserves). For the first time, we examined whether these constraints differ between eggs within clutches and between egg components (yolk and albumen). The interval between colony return and clutch initiation positively influenced the yolk mass, the albumen mass, and the subsequent total egg mass of first-laid eggs. This time interval had only a slight negative influence on the yolk mass of second-laid eggs and no influence on their albumen and subsequent total masses. For both eggs, female body mass at laying positively influenced albumen and total egg masses. Female investment into the entire clutch was not related to the time in the colony before laying but increased with female body mass. These novel results suggest that the unique intraclutch egg size dimorphism exhibited in Eudyptes penguins, with first-laid eggs being consistently smaller than second-laid eggs, might be due to a combination of constraints: a migratory carry-over effect on the first-laid egg and a body reserve depletion effect on the second-laid egg. Both these constraints might explain why the timing of reproduction, especially egg formation, is narrow in migratory capital breeders.