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

Abstract

The evolution of different life-history strategies has been suggested as a major force constraining physiological mechanisms such as immunity. In some long-lived oviparous species, a prolonged persistence of maternal antibodies in offspring could thus be expected in order to protect them over their long growth period. Here, using an intergenerational vaccination design, we show that specific maternal antibodies can display an estimated half-life of 25 days post-hatching in the nestlings of a long-lived bird. This temporal persistence is much longer than previously known for birds and it suggests specific properties in the regulation of IgY immunoglobulin catabolism in such a species. We also show that maternal antibodies in the considered procellariiform species are functional as late as 20 days of age. Using a modelling approach, we highlight that the potential impact of such effects on population viability could be important, notably when using vaccination for conservation. These results have broad implications, from comparative immunology to evolutionary eco-epidemiology and conservation biology.

Figure 1.

Decay of specific anti-NDV antibody levels in chicks from mothers exposed to NDV vaccine for three different bird species, the quail (green), the black-legged kittiwake (blue) and the Cory's shearwater (red). The standardized percentage of inhibition (PI) is presented on the y-axis; 0 represents the negative threshold. The lines correspond to the mean for each species estimated using generalized additive mixed models (GAMM), and the coloured regions around the means represent the associated 95% CI of the slopes.

Figure 2.

Specific anti-NDV antibody levels in 20 days post-hatch Cory's shearwater chicks from vaccinated mothers as a function of their mother anti-NDV antibody level at the time of laying (r_20d = 0.91, n = 12, p < 0.001).

Figure 3.

Specific anti-NDV antibody levels in Cory's shearwater chicks for four treatment groups: chicks from control females, non-vaccinated (blue) and vaccinated when 20 days old (green); chicks from vaccinated females, non-vaccinated (red) and vaccinated when 20 days old (orange). GAMM are used to control for individual effect and nonlinear dynamics. Means and 95% CI of the slopes of the models are presented.

Figure 4.

Dynamics of a hypothetical albatross population under scenarios of exposure to a disease agent deleterious to nestlings and against which an antibody-based vaccine would exist. Dashed curve: when there is no exposure to the disease agent in the population, the population is maintained stable by density-dependent reproduction. Grey curve: when there is no maternal protection or when maternal protection vanishes before an annual epidemic of the disease agent (half-life of maternal antibodies shorter than 10 days, including the 5 days reported for quail and kittiwake), the population is driven towards extinction on a short time scale even if adult females are vaccinated. Black curve: a vaccination coverage of 40% of the sensitive breeding females associated with a sufficiently long half-life of maternal antibodies in offspring (over 10 days, thus including the 24.75 days half-life reported for Cory's shearwater) can dramatically dampen the effects of the annual epidemic and prevent local extinction. Parameters: adult annual survival rate: 0.95; subadult annual survival rate: 0.87; juvenile annual survival rate: 0.7; parasite-induced chick mortality: 0.7; fecundity rate: 0.3 female/female. Initial population size corresponds to the equilibrium population size and age structure at carrying capacity.

Figure 5.

Effect of the vaccination coverage on the size of a hypothetical albatross population at the end of the evaluation (300 years) for various levels of parasite-induced chick mortality. Reasonable vaccination efforts have a strong rescue effect on the population: after a first year of high vaccination effort (60–70 females), the vaccination of only a few (generally 1 or 2) sensitive adult females is needed each year to maintain a vaccination coverage of 40% of the adult females. Parameters: adult annual survival rate, 0.95; subadult annual survival rate, 0.87; juvenile annual survival rate, 0.7; fecundity rate, 0.3 female/female; half-life of maternal antibodies = 25 days. Initial population size corresponds to the equilibrium population size and age structure at carrying capacity.