Evidence of an interannual effect of maternal immunization on the immune response of juveniles in a long‐lived colonial bird

Abstract

Summary 1.Little is known about the maternal transfer of antibodies in natural host-parasite systems despite its possible evolutionary and ecological implications. In domestic animals, the maternal transfer of antibodies can enhance offspring survival via a temporary protection against parasites, but it can also interfere with the juvenile immune response to antigens. 2. We tested the functional role of maternal antibodies in a natural population of a long-lived colonial seabird, the kittiwake ( Rissa tridactyla ), using a vaccine (Newcastle disease virus vaccine) to mimic parasite exposure combined with a cross-fostering design. 3. We first investigated the role of prior maternal exposure on the interannual transmission of Ab to juveniles. We then tested the effect of these antibodies on the juvenile immune response to the same antigen. 4. The results show that specific maternal antibodies were transferred to chicks 1 year after maternal exposure and that these antibodies were functional, i.e. they affected juvenile immunity. These results suggest that the role of maternal antibodies may depend on the timing and pattern of offspring exposure to parasites, along with the patterns of maternal exposure and the dynamics of her immune response. 5. Overall, our approach underlines that although the transgenerational transfer of antibodies in natural populations is likely to have broad implications, the nature of these effects may vary dramatically among host-parasite systems, depending on the physiological mechanisms involved and the ecological context.

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).…”

“…; shearwater: 0.31, kittiwake: 0.30 and quail: 0.22). In addition, in shearwaters, a subset of chicks was vaccinated when 20 days old (n ¼ 11 chicks from control mothers, n ¼ 5 chicks from vaccinated mothers) in order to investigate whether persistent anti-NDV maternal antibodies might block a response to vaccination, as previously shown for other species [21].…”

“…Fieldwork with Cory's shearwaters was conducted in Gran Canaria (15847 0 18 00 N; 27850 0 41 00 E, Canary Archipelago, Spain) in 2010. 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.…”

Antibodies to Influenza A Virus in Wild Birds across Mongolia, 2006–2009

“…However, as maternally derived antibodies to AI virus decrease to zero in 3-4 wk posthatching (Maas et al, 2011), and the age of sampled Mongolian Gulls was greater than 5 wk old, then the antibodies detected in this age class most likely represent exposure to virus at the natal site. Transfer of AI virus specific maternal antibodies is known to catabolize within 2 wk posthatching in Kittiwakes (Rissa tridactyla; Staszewski et al, 2007); thus, chicks should be susceptible to infection thereafter. Second, based on the corresponding viral isolation/RT-PCR data, the results show consistent patterns of seroconversion at natal site (Velarde et al 2010).…”