Antibody injection in the egg yolk: maternal antibodies affect humoral immune response of the offspring

Abstract

Summary1. In vertebrate species, maternal antibodies specific for the pathogens to which mothers have been exposed can be transmitted to offspring before birth. This is assumed to be adaptive as these antibodies can be essential in protecting offspring early in life before their own immune system is fully developed. However, fitness consequences in natural conditions and the long-term effects of these mechanisms have yet to be fully examined. 2. Exploring the ecological and evolutionary implications of such maternal effects requires experimental manipulations to avoid potential confounding maternal effects. In birds, maternal antibodies are transmitted via the egg yolk -a self contained embryonic environment in which antibodies can be manipulated independently outside the maternal environment. 3. Here we use a novel technique to extract and experimentally manipulate maternal antibodies in the egg. Using the common quail (Coturnix coturnix), we demonstrate a blocking effect of antigen specific maternal antibodies received via egg injection, on the offspring's antibody response to an immune challenge with this antigen. Our results also suggest lower antibody production after a second immune challenge if maternal antibodies were present during first infection. 4. Maternal antibodies thus have the potential to affect the development of offspring immunity. Our innovative technique will enable further work to manipulate the transfer of maternal antibodies per se whilst controlling for confounding effects linked to maternal vaccination. Because it also enables to manipulate the amount of antibodies transferred, it will facilitate further study of their adaptive value and ecological consequences in natural host-parasite systems.

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

“…As in quails and kittiwakes [21,29], the antibody levels in females of Cory's shearwaters showed a positive correlation with chick levels soon after hatching (Pearson's correlation coefficient at 5 days of age: r 5d ¼ 0.81, n ¼ 17 chicks from vaccinated mothers, p , 0.001). Importantly, this correlation between females and chicks antibody levels lasted throughout the rearing period in shearwaters despite decreasing numbers of chicks owing to natural mortality during rearing and the use of a sub-sample of chicks for testing a late blocking effect (figure 2; at 10 days of age, r 10d ¼ 0.95, n ¼ 17; at 20 days of age, r 20d ¼ 0.91, n ¼ 12; at 30 days of age, r 30d ¼ 0.91, n ¼ 12, at 40 days of age, r 40d ¼ 0.91, n ¼ 9, p , 0.001 and at 65 days of age, r 65d ¼ 0.72, n ¼ 8, p ¼ 0.042).…”

“…This blocking effect suggests that maternal antibodies are functional as late as 20 days after hatching in shearwaters. By contrast, quail chicks that received maternal antibodies mounted an immune response after vaccination at 20 days of age [29].…”

“…The experiment with kittiwakes took place in Northern Norway [21]. Quails were bred in Konnevesi Research Station (University of Jyväskylä, Finland; [29]). …”

“…This is perhaps because experimentally assessing such a role requires a specific challenge of mothers before breeding and the monitoring of the dynamics of specific maternal antibodies in offspring via repeated sampling during the subsequent rearing period. Although such studies would greatly benefit from considering species with contrasting life histories, to date, data are mostly available for relatively fast-living species, precocial or altricial [14,16,[21][22][23]29,30]. Some studies on long-lived species, such as the California condor (Gymnogyps californianus), suggest a longer maternal protection [24], but design limitations do not permit a clear interpretation of the dynamics of maternal antibody decay.…”

Immune responses link parasite genetic diversity, prevalence and plumage morphs in common buzzards

“…Hanssen et al 2005;Råberg et al 2000), but maternal antibodies may unspecifically block antigens. This could inhibit the stimulation of specific antibody production in the first weeks of a nestling's life and create an opportunity for early incoming parasites such as Leucocytozoon (Staszewski and Siitari 2010). Thus, potentially, dark mothers could transfer the highest amount of antibodies to their nestlings.…”