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Changes in phytohaemagglutinin skin-swelling responses during the breeding season in a multi-brooded species, the Eurasian Tree Sparrow: do males with higher testosterone levels show stronger immune responses?

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Abstract

Life-history theory assumes that the fitness costs of immunity may have negative effects on reproductive success. Similarly, the immunocompetence handicap hypothesis is based on findings that testosterone (T) has immunosuppressive effects, although the basis of this hypothesis has recently been challenged. As much of the work examining the relationship between T levels and immune function has been carried out in captive-housed species, these results may not accurately reflect the situation of animals living in natural environments. To better understand the relationship between plasma T levels and immune function, studies focusing on free-living animals are needed. A previous study by our group determined the changes in both baseline and stress-induced T levels in free-living Eurasian Tree Sparrows (Passer montanus) across different annual cycle stages. In this study, we further report the phytohaemagglutinin skin-swelling (PHA) immune response in this multi-brooded species during different breeding sub-stages, and then determine the relationships between the PHA response and both baseline and stress-induced T levels. Our results show that the PHA response varied across the different sub-stages and differed significantly between the first and second brood stage. Furthermore, T levels in male Tree Sparrows are positively correlated with the PHA response during the breeding season, whereas this relationship is negative in females, suggesting that the biological function of T differs between the sexes. Therefore, our results suggest that free-living animals have evolved the ability to orchestrate trade-offs between reproduction and immune functions based on changes in physiology and the environment, which should provide further opportunities to study the flexibility and plasticity of physiological and ecological adaptations in natural environments.

Zusammenfassung

Unterschiedliche Immunantworten anhand Phytohaemagglutinin-Hautschwellung bei Feldsperlingen während der Brutzeit: Zeigen Männchen mit höheren Testosteronwerten stärkere Immunantworten?

Die “Life-history”-Theorie besagt, dass die Kosten für Fitness des Immunsystems negative Auswirkungen auf den Reproduktionserfolg haben können. In gleicher Weise basiert die Immunkompetenz-Handicap-Hypothese darauf, dass Testosteron (T) immunsuppressive Effekte hat, wobei die Basis dieser Hypothese jüngst in Frage gestellt wurde. Da die meisten Arbeiten den Zusammenhang zwischen T-Levels und Immunfunktion an Arten in Gefangenschaft untersucht wurden, spiegeln die dort erzielten Ergebnisse nicht unbedingt die Situation wild lebender Tiere in ihren natürlichen Lebensräumen wider. Um den Zusammenhang zwischen T-Werten im Blutplasma und der Immunfunktion besser zu verstehen, sind Studien an frei lebenden Tieren notwendig. Eine frühere Studie unserer Arbeitsgruppe bestimmte die Veränderungen sowohl der Basis-Testosteronwerte als auch der stressinduzierten Werte bei freilebenden Feldsperlingen zwischen verschiedenen Phasen im Jahreszyklus. In der vorliegenden Studie dokumentieren wir die Immunantwort durch Phytohämagglutinin Hautschwellung (PHA) von Feldsperlingen während unterschiedlicher Brutstadien und bestimmten anschließend die Verhältnisse zwischen der PHA Immunantwort und den Basis- wie stressinduzierten T-Werte. Die Ergebnisse zeigen, dass die PHA Antwort zwischen verschiedenen Brutstadien variiert und sich signifikant zwischen der ersten und zweiten Brutphase unterscheidet. Darüber hinaus waren die T-Werte der Männchen positive korreliert mit der PHA Anwort während der Brutsaison, wohingegen das Verhältnis bei den Weibchen negativ ist. Das deutet auf eine unterschiedliche biologische Funktion von Testosteron für die Geschlechter hin. Daher weisen unsere Ergebnisse daraufhin, dass wildlebende Tiere die Fähigkeit entwickelt haben, den Konflikt zwischen Reproduktion und Immunfunktionen, basierend auf physiologischen und Umweltveränderungen, abzustimmen. Diese Ergebnisse sollten Anlass dazu geben, die Flexibilität und Plastizität physiologischer und ökologischer Anpassungen in natürlichen Lebensräumen weiter zu untersuchen.

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Acknowledgments

We are very grateful to Xianzhao Zhou, Xiaofei Ma, Ji Zhang, Chenyang Hao for their expert assistance with field and laboratory work. This research was supported by the National Natural Science Foundation of China (NSFC, 31000191; 31330073), the Postdoctoral Science Foundation of China (2011M500537), and the Natural Science Foundation of Hebei Province (NSFHB, 2012205018) to Dongming Li, and NSFHB (2013205018) to Yuefeng Wu.

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  1. Key Laboratory of Animal Physiology, Biochemistry and Molecular Biology of Hebei Province, College of Life Sciences, Hebei Normal University, Shijiazhuang, 050024, China

    Dongming Li, Yinchao Hao, Xuelu Liu, Yao Yao, Chao Du, Xiaorui Zhang, Shuo Cui, Lina Wu & Yuefeng Wu

  2. Department of Biology and Chemistry, Xingtai University, Xingtai, 054001, China

    Lina Wu

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  1. Dongming Li
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Communicated by K. C. Klasing.

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Li, D., Hao, Y., Liu, X. et al. Changes in phytohaemagglutinin skin-swelling responses during the breeding season in a multi-brooded species, the Eurasian Tree Sparrow: do males with higher testosterone levels show stronger immune responses?. J Ornithol 156, 133–141 (2015). https://doi.org/10.1007/s10336-014-1104-2

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