Initial levels of maternally derived antibodies predict persistence time in offspring circulation

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ORIGINAL ARTICLE

Initial levels of maternally derived antibodies predict persistence time in offspring circulation Jennifer L. Grindstaff

Received: 13 May 2009 / Revised: 26 August 2009 / Accepted: 26 October 2009 / Published online: 16 November 2009 Ó Dt. Ornithologen-Gesellschaft e.V. 2009

Abstract Vertebrate mothers transmit antibodies to offspring that provide humoral immunity early in life. The duration of protection provided by maternal antibodies varies considerably among species and has not been widely examined in birds. Determination of the length of maternal protection can be a useful predictor of when young are most likely to be susceptible to infection. The duration of maternal antibody protection was determined in Japanese Quail (Coturnix japonica) by immunizing females with keyhole limpet hemocyanin (KLH) and then collecting blood samples from offspring. Maternal antibodies remained detectable in offspring circulation for an average of 14 days (range 3–28). The duration of persistence was predicted by antibody levels as measured in maternal circulation, within egg yolks, or measured in offspring shortly after hatch. Thus, the primary benefit to offspring of high concentrations of maternal antibodies is likely to be an extended period of maternal protection during early growth and development. Keywords Antibody persistence  Ecological immunology  Immunocompetence  Maternal antibody transmission  Maternal effects  Passive immunity

Communicated by C. G. Guglielmo. J. L. Grindstaff Department of Biology, Center for the Integrative Study of Animal Behavior, Indiana University, 1001 E. Third Street, Bloomington, IN 47405, USA Present Address: J. L. Grindstaff (&) Department of Zoology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078, USA e-mail: [email protected]

Introduction Maternal antibody transmission provides the primary form of humoral immune defense for young vertebrates (Brambell 1970; Grindstaff et al. 2003). Antibody concentration and diversity are generally correlated between mothers and their offspring early in life (Graczyk et al. 1994; Bollen and Hau 1999; Gasparini et al. 2002; Grindstaff 2008). The concentration and diversity of antibodies transmitted may consequently influence the disease resistance and survival probability of offspring (Smith et al. 1994; Sahin et al. 2003; Al-Natour et al. 2004). Maternal antibodies are rapidly catabolized from offspring circulation after birth or hatch (Brambell 1970; Grindstaff et al. 2003). Passively transmitted antibodies are cleared at an exponential rate from offspring circulation (Nicoara et al. 1999). Offspring with higher initial levels of maternal antibodies generally retain maternal immunity longer than offspring with low initial levels of maternal antibodies (Smith et al. 1994). Young generally lose maternal protection before mature adult levels of humoral immunity are generated endogenously (Solomon 1971; Klasing and Leshchinsky 1999). Thus, offspring may be most susceptible to infectious diseases dur