Are Maternal Antibodies Really That Important? Patterns in the Immunologic Development of Altricial Passerine House Sparrows (Passer domesticus)

Abstract

BackgroundMaternal antibodies are believed to play an integral role in protecting immunologically immature wild-passerines from environmental antigens. This study comprehensively examines the early development of the adaptive immune system in an altricial-developing wild passerine species, the house sparrow (Passer domestics), by characterizing the half-life of maternal antibodies in nestling plasma, the onset of de novo synthesis of endogenous antibodies by nestlings, and the timing of immunological independence, where nestlings rely entirely on their own antibodies for immunologic protection.Methodology/Principal FindingsIn an aviary study we vaccinated females against a novel antigen that these birds would not otherwise encounter in their natural environment, and measured both antigen-specific and total antibody concentration in the plasma of females, yolks, and nestlings. We traced the transfer of maternal antibodies from females to nestlings through the yolk and measured catabolisation of maternal antigen-specific antibodies in nestlings during early development. By utilizing measurements of non-specific and specific antibody levels in nestling plasma we were able to calculate the half-life of maternal antibodies in nestling plasma and the time point at which nestling were capable of synthesizing antibodies themselves. Based on the short half-life of maternal antibodies, the rapid production of endogenous antibodies by nestlings and the relatively low transfer of maternal antibodies to nestlings, our findings suggest that altricial-developing sparrows achieve immunologic independence much earlier than precocial birds.Conclusions/SignificanceTo our knowledge, this is the first in depth analyses performed on the adaptive immune system of a wild-passerine species. Our results suggest that maternal antibodies may not confer the immunologic protection or immune priming previously proposed in other passerine studies. Further research needs to be conducted on other altricial passerines to determine if the results of our study are a species-specific phenomenon or if they apply to all altricial-developing birds.

Maternal Antibody Transfer Can Lead to Suppression of Humoral Immunity in Developing Zebra Finches (Taeniopygia guttata)

“…These data likely document the pattern of endogenous production of total Ig in developing zebra finches rather than changes in maternally transferred antibody or endogenous production of LPS- or KLH-reactive IgY. Maternal antibodies typically peak in the first 2–5 d posthatch (reviewed in Davison et al 2008) and are then catabolized over the first 14 d posthatch in most altricial species studied (Lozano and Ydenberg 2002; Nemeth et al 2008; King et al 2010). The subsequent increase in total Ig levels likely reflects production of natural antibodies, which does not require antigen exposure (Davison et al 2008).…”

Ontogeny of constitutive immunity: maternal vs. endogenous influences

“…Maternal antibodies may contribute to early immune function in altricial birds, but persist only a few days in nestling plasma in passerine birds (Nemeth, Oesterle & Bowen ; King, Owen & Schwabl ; but see Garnier et al . for long‐lived sea birds).…”

“…; Reid et al . ; King, Owen & Schwabl ) and activity of constitutive components within the first weeks after hatching in species with an altricial mode of development (Mauck et al . ; Palacios et al .…”

Injecting the mite into ecological immunology: measuring the antibody response of house sparrows (Passer domesticus) challenged with hematophagous mites

“…Mite-specific antibody assays.-A secondary antibody used to detect House Sparrow immunoglobulins was produced following the published protocol described independently by Huber et al (2010) and King et al (2010). Briefly, House Sparrow immunoglobulin Y (HOSP-IgY) was isolated from House Sparrow yolks using thiophilic interaction chromatography (Hansen et al 1998).…”

“…Plates were standardized to control between-plate variations in absorbance following the methods described by Hubert et al (2010) and King et al (2010). Prior to standardization, the OD of the NSB was subtracted from the OD of each sample and control, per plate.…”