Prenatal and postnatal parental effects on immunity and growth in ‘lactating’ pigeons

Abstract

Summary1. 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.

Telomere erosion varies with sex and age at immune challenge but not with maternal antibodies in pigeons

“…One month later, a second injection of antigens or saline was performed to increase differences in circulating antibody level of parents. Antigen‐injected biological mothers transmitted more maternal anti‐KLH antibodies to their nestlings (MatAb+ nestlings), compared with sham‐injected biological mothers (MatAb− nestlings) as shown in a previous study (Jacquin, Blottiere, Haussy, Perret, & Gasparini, ). The day of a clutch completion, the first egg of each clutch was collected for antibody assay and the second egg was cross‐fostered with another nest of similar laying date.…”

“…Twenty‐two chicks received an early injection soon after hatching, at the age of 3 days (early‐injected chicks: 11 females, 11 males) and 25 other chicks received a late injection after hatching at the age of 14 days (late‐injected chicks: 16 females, nine males). Eleven days after injection, we took blood samples from the brachial vein and anti‐KLH antibody levels in the plasma were determined using a sandwich ELISA (Hasselquist et al., as described in Jacquin et al., ). Additionally, all chicks came from the second egg in this study, and were raised alone, because the first egg was sampled for antibody assay.…”

Eco-Evolutionary Dynamics

“…Isaksson et al, 2006) and transmission of immune factors (e.g. Jacquin et al, 2012;Roth et al, 2012) exist in the literature. In addition, females can alter their investment in offspring in response to males' characteristics (e.g.…”

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

“…This allowed the determination of the dynamics of maternal antibodies in the chick plasma to ultimately investigate the interannual dynamics of the transfer and the persistence of maternal antibodies in the chicks. To explore the potential of parental provisioning as an alternative antibody transfer route (e.g., Prevost 1962;Jacquin et al 2012), in 2012 we also sampled stomach oil from ten 5-day-old chicks (five chicks from vaccinated mothers in 2010 and five chicks from nonvaccinated mothers), using blunt-ended 5-mm-diameter plastic cannula attached to a suction bulb (Janssens et al 1999). Additionally, throughout the study period, we opportunistically sampled a few egg yolks from deserted burrows (i.e., nonvisited for 15 days) for which we had already sampled the females (three from vaccinated females and three from control females).…”