Maternal antibodies reduce costs of an immune response during development

Abstract

SUMMARYYoung vertebrates are dependent primarily on innate immunity and maternally derived antibodies for immune defense. This reliance on innate immunity and the associated inflammatory response often leads to reduced growth rates after antigenic challenge. However, if offspring have maternal antibodies that recognize an antigen, these antibodies should block stimulation of the inflammatory response and reduce growth suppression. To determine whether maternal and/or offspring antigen exposure affect antibody transmission and offspring growth, female Japanese quail (Coturnix japonica) and their newly hatched chicks were immunized. Mothers were immunized with lipopolysaccharide (LPS), killed avian reovirus vaccine (AR), or were given a control, phosphate-buffered saline, injection. Within each family, one-third of offspring were immunized with LPS, one-third were immunized with AR, and one-third were given the control treatment. Maternal immunization significantly affected the specific types of antibodies that were transmitted. In general, immunization depressed offspring growth. However, offspring immunized with the same antigen as their mother exhibited elevated growth in comparison to siblings immunized with a different antigen. This suggests that the growth suppressive effects of antigen exposure during development can be partially ameliorated by the presence of maternal antibodies, but in the absence of specific maternal antibodies, offspring are dependent on more costly innate immune defenses. Together, the results suggest that the local disease environment of mothers prior to reproduction significantly affects maternal antibody transmission and these maternal antibodies may allow offspring to partially maintain growth during infection in addition to providing passive humoral immune defense.

Vaccination in Nile tilapia broodstock with whole cell vaccine and disease resistance in its fry against Aeromonas hydrophila

“…This suggests that specific antibody play an important role in fish protection against pathogenic infection. Maternal antibody from the broodstock fish can reduce the risk of mortality rate during the development of fry fish (Grindstaff, 2008).…”

Growth and innate immunity are not limited by selection for high egg testosterone content in Japanese quail

“…For now, it is not clear whether these elevated antibody concentrations reflect higher maternal antibody transfer, enhanced activity of offspring's own immune system or a combination of both. In Japanese quail, maternal antibodies decline between 6 and 11days post-hatching, and thus the synthesis of endogenous antibodies seems to be independently active only after this age (Grindstaff, 2008). The maternal antibodies persist in the circulation of quail chicks during the first 30days of life (Grindstaff, 2010), and over this period they can provide passive protection against pathogenic agents the mother encountered during her prior life (Brambell, 1970), prime the humoral immune response (Gasparini et al, 2006;Reid et al, 2006) and reduce the costs of antigen challenges associated with growth suppression (Grindstaff, 2008).…”

“…In addition, we measured basal levels of non-specific antibodies (IgY) in the circulation of chicks. These immunoglobulins may be of both maternal and endogenous origin because maternal antibodies pass through the yolk into the embryo (Brambell, 1970) and endogenous IgY-bearing cells have been detected during the embryonic development (Kincade and Cooper, 1971), although endogenous synthesis of antibodies begins to dominate after 2weeks of age (Watanabe and Nagayama, 1979;Grindstaff, 2008). Artificial selection for yolk T concentrations has proved a heritable variation of yolk hormone transfer accounting for nearly half of its total phenotypic variance (Okuliarova et al, 2011b).…”

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

“…Different studies have demonstrated in birds that an immune challenge during development was responsible for a reduction in the growth rate [25,26], which is known to influence the fitness of nestlings [27]. However, those studies have mostly focused on innate immune mechanisms, and the potential role of the transfer of maternal antibodies as a mechanism favouring chick growth in the face of parasitic challenge has often been neglected (but see [28]). 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.…”