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1. Parental effects can have profound consequences on offspring phenotype. Still, little is known about the relative influence of prenatal versus postnatal parental effects of parasite exposure of parents on offspring traits.
2. In this study, we investigated the respective role of a prenatal and a postnatal immune challenge of parent feral pigeons (Columba livia) on offspring humoral immunity, growth and survival. We used a cross-fostering design and antigen injections in biological and foster parents. Feral pigeons are particularly suitable for studying the effects of parental immune challenges because they can affect the phenotype of their young through the transmission of prenatal antibodies in the egg and postnatal antibodies in the ‘crop milk’, a substance produced in the crop of both parents.
3. Results show that a prenatal immune challenge of biological parents with keyhole limpet haemocyanin (KLH) antigen decreased the humoral response against KLH of nestlings injected at 14 days of age. In contrast, a postnatal immune challenge of foster parents with KLH enhanced the humoral response of 1-year-old juveniles exposed to a second KLH injection, but only when these juveniles had received their first injection at 3 days of age.
4. No effect on nestling and juvenile response to another antigen (NDV) was observed, indicating that the changes in humoral responses were specific to the KLH injected in parents. In addition to this, prenatal and postnatal parental immune challenges had an interaction effect on fledging body mass, but no effect on juvenile survival.
5. This study shows that pre- and postnatal exposure to antigens in parents has contrasted effects on offspring humoral response and growth. Moreover, it shows that the timing of an early exposure to antigens in nestlings has important effects on their specific humoral response.
6. This study thus suggests that pre- and postnatal parental effects have distinct roles in shaping the phenotype of the offspring on different time scales and calls for further investigations on the potential adaptive role of combined parental effects. Moreover, it suggests that pigeon milk has positive effects on offspring humoral immunity and thus could potentially have a similar immune role as mammalian milk.
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Parental effects are now recognized as a major source of transgenerational phenotypic plasticity that has short-term and long-term consequences on offspring ontogeny and fitness (Mousseau & Fox 1998). In the context of ecological immunology, maternal exposure to parasites at the time of breeding can profoundly affect maternal effects in different ways. For instance, an immune challenge with artificial antigens can indirectly affect parental effects as it is now well established that mounting an immune response is costly and can negatively impact the intensity of parental investment (Bonneaud et al. 2003). In addition, an immune challenge can directly affect parental effects by the transfer of specific antibodies from mothers to offspring, which are known to affect several aspects of offspring phenotype (Grindstaff, Brodie & Ketterson 2003; Boulinier & Staszewski 2008; Hasselquist & Nilsson 2009). Indeed, maternal antibodies can confer a transient protection of the young against parasites and can therefore have positive effects on offspring survival (Heeb et al. 1998). They also have profound effects on offspring immune ontogeny, through positive influences on the intensity of the humoral response and on the ontogeny of the immune system (educational effects, Gasparini et al. 2006; Grindstaff et al. 2006; Reid et al. 2006), but also through transient blocking effects on the young immune response, because high levels of maternal antibodies can suppress the stimulation of the immune system (blocking effect, Staszewski et al. 2007; Staszewski & Siitari 2010). Furthermore, maternal antibodies have been shown to positively affect offspring growth, likely through reallocation of energy of offspring from costly immune response to growth (Robison, Stott & DeNise 1988).
Maternal antibodies can be transmitted through two main routes: before the birth of the young (prenatal antibody transmission) or after the birth (postnatal antibody transmission) (Boulinier & Staszewski 2008). Prenatal antibodies are mainly Immunoglobulins Y (IgY) contained in avian eggs and IgG transmitted through the placenta in mammals (Chucri et al. 2010). Birds are ideal models to study the prenatal transmission of antibodies because the mother can potentially modulate the amount of antibodies transferred in the egg yolk (Saino et al. 2002; Hasselquist & Nilsson 2009). Such prenatal antibodies have been shown to affect several fitness parameters in offspring (reviewed in Grindstaff, Brodie & Ketterson 2003; Hasselquist & Nilsson 2009). In contrast, mammals are ideal models to study the postnatal transmission of antibodies through the colostrum and breast milk (e.g. Marquez et al. 2003). Such postnatal antibodies provide offspring with protection against diseases in humans (Van de Perre 2003; Hanson 2007), domestic animals (reviewed in Grindstaff, Brodie & Ketterson 2003) and potentially in wild animal populations (Graham et al. 2010). Colostrum and milk of some mammals like humans or rabbits are mainly composed of immunoglobulins A (IgA), which are believed to play a central role in gut protection against local infections (Van de Perre 2003) and potentially in immune function priming (Hanson 1998). Indeed in mammals, antibodies transmitted postnatally seem to have a parallel but distinct role compared with antibodies transmitted prenatally (Morshed et al. 1993). However, few studies have been able to disentangle the respective role of pre- and postnatal antibodies in animals and their evolutionary consequences in wild populations.
Both prenatal and postnatal maternal effects are indeed likely to play a role in the evolution of natural systems (Biard, Surai & Møller 2006). To better understand the evolutionary consequences of the prenatal and postnatal effects of parental exposure to parasites, we need to investigate the direct and indirect consequences of an immune challenge in parents on offspring phenotype. Columbidae, such as feral pigeons Columba livia (Fig. 1), are ideal models to address this question. Indeed, parent and offspring free-living feral pigeons share the risk of exposure to the same deleterious parasites (such as Chlamydia psitacci and Trichomonas), which are responsible for a high nestling and subadult mortality (30% and 50%, respectively, Johnston & Janiga 1995). In this context, the transmission of maternal antibodies to the young may have strong positive effects on offspring fitness by conferring a protection against such parasites through direct protective effects of maternal antibodies and/or through an enhancement of offspring immune defence (Heeb et al. 1998; Kallio et al. 2006; Nemeth & Bowen 2007, but see Addison, Ricklefs & Klasing 2010).
Moreover, adult pigeons feed their chicks with a lipid-rich substance produced in their crop, named crop milk (Johnston & Janiga 1995). It is known to contain nutrients, minerals and growth factors (Shetty et al. 1992), but also immune active substances such as carotenoids (Eraud et al. 2008) and immunoglobulins (Engberg et al. 1992). This model offers us a unique chance to disentangle the effects of a prenatal immune challenge (inducing the transmission of prenatal egg antibodies through the yolk), and of a postnatal immune challenge (inducing the transmission of postnatal antibodies through the crop milk) on offspring phenotype. Although the production of milk is quite an exception in birds (it is known only in Columbids: Goodwin 1977; emperor penguins: Prevost 1962 and flamingos: Studer-Thiersch 1967), it is suspected that other altricial birds feeding their young by oral regurgitation (like vultures or swifts) could also potentially transfer salivary antibodies to their offspring (Apanius 1998).
In this study, we aimed to unravel the respective importance of prenatal and postnatal parental effects on growth, humoral immune response and survival of chicks following an immune challenge. To this end, we injected selected adult feral pigeons with an antigen (keyhole limpet haemocyanin, KLH) and swapped eggs between nests, allowing us to obtain chicks with only a prenatal parental immune challenge, only a postnatal parental immune challenge, both postnatal and prenatal or no parental immune challenge. We then recorded the short-term and long-term effects of these parental treatments on offspring humoral immune response against two antigens (KLH and NDV), as well as on their growth and survival. Because we did not directly manipulate parental antibodies in eggs or milk, the effect of parental antibodies on chick humoral response may be confounded by parental effects that affect the whole offspring immune system (Grindstaff et al. 2006). To ensure that effects observed on the humoral response were mediated by specific parental antibodies, we considered not only the humoral response of offspring against KLH, but also their humoral response against NDV, an antigen to which parents were not exposed. If the effects mediated by maternal antibodies are specific to the antigen injected in parents, we expect to find different effects of parental immunization on offspring humoral response against KLH and NDV antigens.