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.

Long Antibody Persistence and Transgenerational Transfer of Immunity in a Long-Lived Vertebrate

“…We modeled the dynamics of anti-NDV antibody levels in vaccinated, revaccinated, and nonvaccinated females (females ϩ , females ϩϩ , and females Ϫ , respectively), using generalized additive mixed models (GAMMs; see Garnier et al 2012b). We used the library mgcv in R (R Development Core Team 2010), on the basis of penalized regression splines and generalized cross-validation to select the appropriate smoothing parameters (Wood and Augustin 2002).…”

“…Most studies so far have focused on humans, livestock and poultry species, model laboratory animals, and relatively fast-living species (Feuer et al 1999;Frank 2002;Beal et al 2004;Bunikis et al 2004;Gibbs et al 2005;Kuenzi et al 2005;Henning et al 2006;Amanna et al 2007;Tizard 2013). In addition, the few studies of long-lived species usually lack the longitudinal dimension necessary to assess how immune responses vary over the course of a life span (Sandland and Minchella 2003;Chang et al 2007;Guiserix et al 2007; Lecomte et al 2010;Garnier et al 2012b). One mechanism that offers the potential for such studies is the transgenerational transfer of antibodies from mothers to offspring.…”

“…However, although the dynamics of the transferred antibodies in the offspring is well described in mammals, it remains relatively poorly studied in birds. For instance, a recent study in a long-lived seabird species showed that maternal antibodies can persist several weeks after hatching (Garnier et al 2012b), much longer than previously thought for any bird species (Davison et al 2008). Because initial levels of antibodies in the newborn depend on maternal levels (Gasparini et al 2001(Gasparini et al , 2002 and in turn determine their persistence (Grindstaff 2010), the temporal dynamics of antibody levels in adults represents highly valuable information.…”

“…The temporal dynamics and the efficacy of the humoral immune response of chickens to these vaccines can vary greatly (e.g., Walker et al 2010), but very little is known about the dynamics of the humoral immune response in long-lived bird species (Bailey et al 1998;Momayez et al 2007;Garnier et al 2012b;Tolf et al 2013). For instance, whether the long persistence of maternal antibodies reported in a long-lived seabird species (Garnier et al 2012b) is associated with the persistence of high antibody levels in adults would be of interest. The immune dynamics of adult females would indeed be expected to affect the initial levels of antibodies passively acquired by chicks and, thus, the duration of protection by maternal antibodies.…”

Immune Response to Newcastle Disease Virus Vaccination in a Wild Passerine

“…Vaccination is a common technique widely applied to prevent and alleviate disease and as an immunologic tool to study eco-epidemiology in wild animal populations (e.g., Staszewski and Boulinier, 2004). The development of new in vivo immunologic methods can improve our understanding of host-pathogen dynamics in the wild, potential pathogen reservoirs, and epizootics that may be crucial for endangered species' survival, and the study of passive immunity (e.g., Garnier et al, 2011).…”