Pre-laying nutrition mediates maternal effects on offspring immune capacity and growth in the pied flycatcher

Abstract

We have aimed at detecting prelaying maternal effects on nestling antibody defences and growth through experimental food supplementation of female pied flycatchers Ficedula hypoleuca and subsequent exchange of whole clutches with control nests. The levels of immunoglobulins and the mass and size of chicks at 12 days of age were ascertained. This is the first study controlling for maternal incubation effects by exchanging eggs rather than nestlings. Our prediction is that the females' availability of pre-laying nutritional resources affects offspring immune capacity and growth through maternal effects in the eggs when conditions during incubation and rearing are controlled for. Nestling immunoglobulin Y (IgY) levels and tarsus length were indeed positively associated with maternal food supplementation at laying. The only rearing environmental effect detected was that of mite infestation which affected both IgY levels and growth of nestlings. Nestlings that recruited to the population in the subsequent 2 years had higher IgY levels than those that did not. Maternal adaptations for allocating resources to eggs play an important role in moulding offspring phenotypes and may affect their survival prospects.

Epigenetics and transgenerational transfer: a physiological perspective

“…These maternally derived factors can have a significant impact on offspring physiological phenotype (i.e. immunological capacity, growth and development, cardiovascular function and toxicant resistance) in a wide range of animals (Munkittrick and Dixon, 1988;Meyer et al, 2003;Weaver et al, 2004;Groothuis et al, 2005;Sellin and Kolok, 2006;Groothuis and Schwabl, 2008;Ho, 2008;Moreno et al, 2008;Romano et al, 2008;Hasselquist and Nilsson, 2009 (Ho, 2008). Metabolic rate, however, was not affected (Ho, 2008).…”

“…maternal supplementation or stress-induced modulation), or that artificially alter yolk factor concentrations report dose-dependent changes in physiological parameters such as stress response, immune capacity, flight performance and growth rate of the offspring. In the pied flycatcher (Ficedula hypoleuca), increased yolk immunoglobulin concentration via maternal nutritional supplementation increased nestling plasma immunoglobulin Y levels and resistance to mite infestation (Moreno et al, 2008), while the transfer of carotenoids (antioxidants) from the female to her offspring in the blue tit (Parus caeruleus) and the grey partridge (Perdix perdix) positively modulates the immune response of nestlings (Biard et al, 2007;Cucco et al, 2008). In contrast, maternal testosterone negatively affects hatchling immune function while enhancing growth in birds and lizards (Groothuis et al, 2005;Cucco et al, 2008).…”

Variation in innate immunity in relation to ectoparasite load, age and season: a field experiment in great tits (Parus major)

“…Furthermore, maternally transferred antibodies in the offspring of many bird species are quickly catabolized and replaced by endogenously synthesized antibodies (Apanius and Nisbet, 2006;Grindstaff et al, 2006;Pihlaja et al, 2006), hence NAb levels measured in 15day old nestlings can be assumed to reflect endogenous antibodies. Yet, it remains possible that maternal transfer of antibodies affects endogenous NAb production of nestlings (see Grindstaff et al, 2006;Moreno et al, 2008;Reid et al, 2006). The fact that female great tits exposed to hen fleas deposit higher levels of IgY into their eggs (Buechler et al, 2002), possibly triggering the higher flea resistance in nestlings originating from nests that already contained fleas during egg laying (Heeb et al, 1998), supports such relationship.…”

Maternal effects as drivers of sibling competition in a parent–offspring conflict context? An experimental test

“…2003; Moreno et al. 2008). This does not necessarily contradict our hypothesis that in intermediate food availability (the Unfed group in our case), mothers benefited by enhancing the competitiveness of their junior chick via maternal effects.…”