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Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity.

ABSTRACT: Young vertebrates have limited capacity to synthesize antibodies and are dependent on the protection of maternally transmitted antibodies for humoral disease resistance early in life. However, mothers may enhance fitness by priming their offspring's immune systems to elevate disease resistance. Transgenerational induced defences have been documented in plants and invertebrates, but maternal priming of offspring immunity in vertebrates has been essentially neglected. To test the ability of mothers to stimulate the immune systems of offspring, we manipulated maternal and offspring antigen exposure in a wild population of birds, pied flycatchers (Ficedula hypoleuca). We show that immunization of the mother before egg laying apparently stimulates a transgenerational defence against pathogens by elevating endogenous offspring antibody production. If the disease environments encountered by mothers and offspring are similar, this transgenerational immune priming may allow young to better cope with the local pathogen fauna.

SUBMITTER: Grindstaff JL

PROVIDER: S-EPMC1634911 | biostudies-literature | 2006 Oct

REPOSITORIES: biostudies-literature

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Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity.

Grindstaff Jennifer L JL Hasselquist Dennis D Nilsson Jan-Ke JK Sandell Maria M Smith Henrik G HG Stjernman Martin M

Proceedings. Biological sciences 20061001 1600

Young vertebrates have limited capacity to synthesize antibodies and are dependent on the protection of maternally transmitted antibodies for humoral disease resistance early in life. However, mothers may enhance fitness by priming their offspring's immune systems to elevate disease resistance. Transgenerational induced defences have been documented in plants and invertebrates, but maternal priming of offspring immunity in vertebrates has been essentially neglected. To test the ability of mother ...[more]

PMID: 16959648

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Project description:In insects, a parental immune challenge can prepare and enhance offspring immune activity. Previous studies of such transgenerational immune priming (TGIP) mainly focused on a single offspring life stage. However, different developmental stages may be exposed to different risks and show different susceptibility to parental immune priming. Here we addressed the question (i) whether TGIP effects on the immunity of Manduca sexta offspring vary among the different developmental offspring stages. We differentiated between unchallenged and immunochallenged offspring; for the latter type of offspring, we further investigated (ii) whether TGIP has an impact on the time that enhanced immune levels persist after offspring immune challenge. Finally, we determined (iii) whether TGIP effects on offspring performance depend on the offspring stage. Our results show that TGIP effects on phenoloxidase (PO) activity, but not on antibacterial activity, vary among unchallenged offspring stages. In contrast, TGIP effects on PO and antibacterial activity did not vary among immunochallenged offspring stages. The persistence of enhanced immune levels in immunochallenged offspring was dependent on the parental immune state. Antibacterial (but not PO) activity in offspring of immunochallenged parents decreased over five days after pupal immune challenge, whereas no significant change over time was detectable in offspring of control parents. Finally, TGIP effects on the developmental time of unchallenged offspring varied among stages; young larvae of immunochallenged parents developed faster and gained more weight than larvae of control parents. However, offspring females of immunochallenged parents laid fewer eggs than females derived from control parents. These findings suggest that the benefits which the offspring gains from TGIP during juvenile development are paid by the adults with reduced reproductive power. Our study shows that TGIP effects vary among offspring stages and depend on the type of immunity (PO or antibacterial activity) as well as the time past offspring immune challenge.

Dataset Information

Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity.

Publications

Transgenerational priming of immunity: maternal exposure to a bacterial antigen enhances offspring humoral immunity.

Similar Datasets

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