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Short- and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch

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Abstract

Hormone-mediated maternal effects play an important role in the formation of a differentiated phenotype. They have been shown to influence a wide array of offspring traits, both early in life and in adulthood. One important offspring trait that is under the influence of maternal androgens is the immune system. In birds, a growing number of studies show that yolk androgens modulate immune function during the chick stage. However, there is a lack of knowledge regarding long-term effects of prenatal androgens on offspring immunity. In this study, we therefore investigated the influence of prenatal testosterone (T) on several measures of immunity in fledgling and adult zebra finches (Taeniopygia guttata). Cell-mediated immune response (towards phytohaemagglutinin, PHA) of fledglings hatching from control eggs was negatively related to brood size, whereas there was no such association for fledglings hatching from eggs with experimentally elevated T levels (T fledglings). Male control fledglings showed reduced mass gain compared to female control fledglings within 24 h after the PHA injection. This pattern was reversed in T fledglings. Total antibody levels in fledglings were not affected by egg treatment. Neither cell-mediated immunity nor total antibody levels in sexually mature zebra finches were influenced by egg treatment. However, there was an immuno-enhancing effect of elevated egg T on both primary and secondary humoral immune responses toward diphtheria and tetanus antigens in ca 5 and 7 month old zebra finches. In addition, the covariation between different immune components differed between T and control offspring, suggesting that egg treatment may have altered the potential trade-offs between different parts of the immune system. Our results suggest that prenatal androgens could be an important factor contributing to individual variation in immune function even in adulthood.

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Acknowledgements

We thank Sandra Chiriac for help with the zebra finches. Two anonymous reviewers provided constructive comments which improved the quality of the manuscript. This study was supported by the Royal Physiographic Society in Lund (to MT), the Swedish Research Council for Environment, Agricultural Science and Spatial Planning (Formas) (to DH) and the Swedish Research Council (to DH and MIS). The experiment was performed with approval from the Malmö/Lund ethical committee for animal research.

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  1. Michael Tobler

    Present address: School of Biological Sciences, University of Wollongong, Northfields Avenue, Wollongong, NSW, 2522, Australia

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  1. Department of Animal Ecology, Lund University, Ecology Building, SE-223 62, Lund, Sweden

    Michael Tobler, Dennis Hasselquist, Henrik G. Smith & Maria I. Sandell

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Correspondence to Michael Tobler.

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Communicated by J. Graves

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Tobler, M., Hasselquist, D., Smith, H.G. et al. Short- and long-term consequences of prenatal testosterone for immune function: an experimental study in the zebra finch. Behav Ecol Sociobiol 64, 717–727 (2010). https://doi.org/10.1007/s00265-009-0889-0

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