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

Abstract

Maternally transferred antibodies have been documented in a wide range of taxa and are thought to adaptively provide protection against parasites and pathogens while the offspring immune system is developing. In most birds, transfer occurs when females deposit immunoglobulin Y into the egg yolk, and it is proportional to the amount in the female’s plasma. Maternal antibodies can provide short-term passive protection as well as specific and nonspecific immunological priming, but high levels of maternal antibody can result in suppression of the offspring’s humoral immune response. We injected adult female zebra finches (Taeniopygia guttata) with one of two antigens (lipo-polysaccharide [LPS] or keyhole limpet hemocyanin [KLH]) or a control and then injected offspring with LPS, KLH, or a control on days 5 and 28 posthatch to examine the impact of maternally transferred antibodies on the ontogeny of the offspring’s humoral immune system. We found that offspring of females exposed to KLH had elevated levels of KLH-reactive antibody over the first 17–28 days posthatch but reduced KLH-specific antibody production between days 28 and 36. We also found that offspring exposed to either LPS or KLH exhibited reduced total antibody levels, compared to offspring that received a control injection. These results indicate that high levels of maternal antibodies or antigen exposure during development can have negative repercussions on short-term antibody production and may have long-term fitness repercussions for the offspring.

Immune Activation Generates Corticosterone-Mediated Terminal Reproductive Investment in a Wild Bird

“…However, whether this constitutes terminal investment or an “anticipatory parental effect” remains unresolved, and its resolution requires a cross-fostering approach to separate pre- from post-natal conditions experienced by offspring. Anticipatory parental effects, or “predictive adaptive responses,” occur when the environment experienced by parents (e.g., risk of parasitism) has epigenetic effects on offspring, potentially matching their phenotype or behavior to the environment offspring are likely to encounter (Saastamoinen et al 2010; Coslovsky and Richner 2011; Crews et al 2012; Uller et al 2013; Burgess and Marshall 2014; Burton and Metcalfe 2014; Merrill and Grindstaff 2014 a , b ). Unlike terminal investment, this hypothesis does not predict an increase in reproductive effort as a response to reduced residual reproductive value.…”

Pre and post-natal antigen exposure can program the stress axis of adult zebra finches: Evidence for environment matching

“…Birds in the LPS treatment were injected with 1.0 mg of LPS/kg body weight (Sigma L7261) in 50 μl of sterilized PBS (n = 20) (Owen-Ashley et al, 2006). These doses have been demonstrated to elicit robust immune responses without leading to prolonged morbidity or mortality (Grindstaff et al, 2012; Merrill and Grindstaff, 2014). Birds in the control treatment were injected with 50 μl of sterilized PBS only.…”

“…Antigen challenge was successful in stimulating the production of antigen-reactive antibody in females and transmission of KLH and LPS specific antibodies to offspring. Furthermore, maternal antigen challenge significantly impacted antibody production by offspring (Merrill and Grindstaff, 2014). …”

“…(from Merrill and Grindstaff, 2014 ). Timeline for pre-natal and post-natal experimental procedures.…”

“…Activation of the immune system can also have long-lasting effects on numerous other traits, including learning and behavior (Bilbo and Schwarz, 2009; Meyer et al, 2009; Grindstaff et al, 2012), growth rates (Klasing and Leshchinsky, 1999; Grindstaff, 2008), immune function (Lemke and Lange, 1999; Grindstaff et al, 2006; Pihlaja et al, 2006; Merrill and Grindstaff, 2014), and endocrine function (Karrow, 2006; Hsiao and Patterson, 2011). One way in which immune activation can affect endocrine function is through the release of cytokines such as IL-1, IL-6, and TNF (Turnbull and Rivier, 1995).…”