Testing the immunocompetence handicap hypothesis: a review of the evidence

Roberts, M.L.; Buchanan, Katherine L.; Evans, Matthew R.

doi:10.1016/j.anbehav.2004.05.001

Cited by 607 publications

(547 citation statements)

References 98 publications

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“…Fargallo et al 2002;Hõrak et al 1999;Saino et al 1997). Second, lower immune responses in large broods might be caused by increased sibling competition resulting in an increase in testosterone (Naguib et al 2004) and a suppressed immune function (Boonekamp et al 2008;Fargallo et al 2007;Folstad and Karter 1992; but see Roberts et al 2004). Evidence for immunosuppressive effects of testosterone, however, is still lacking for zebra finches.…”

Section: Discussionmentioning

confidence: 99%

Effects of early developmental conditions on innate immunity are only evident under favourable adult conditions in zebra finches

Coster

Verhulst

Koetsier

et al. 2011

Naturwissenschaften

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Long-term effects of unfavourable conditions during development can be expected to depend on the quality of the environment experienced by the same individuals during adulthood. Yet, in the majority of studies, long-term effects of early developmental conditions have been assessed under favourable adult conditions only. The immune system might be particularly vulnerable to early environmental conditions as its development, maintenance and use are thought to be energetically costly. Here, we studied the interactive effects of favourable and unfavourable conditions during nestling and adult stages on innate immunity (lysis and agglutination scores) of captive male and female zebra finches (Taeniopygia guttata). Nestling environmental conditions were manipulated by a brood size experiment, while a foraging cost treatment was imposed on the same individuals during adulthood. This combined treatment showed that innate immunity of adult zebra finches is affected by their early developmental conditions and varies between both sexes. Lysis scores, but not agglutination scores, were higher in individuals raised in small broods and in males. However, these effects were only present in birds that experienced low foraging costs. This study shows that the quality of the adult environment may shape the long-term consequences of early developmental conditions on innate immunity, as long-term effects of nestling environment were only evident under favourable adult conditions

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Section: Discussionmentioning

confidence: 99%

Effects of early developmental conditions on innate immunity are only evident under favourable adult conditions in zebra finches

Coster

Verhulst

Koetsier

et al. 2011

Naturwissenschaften

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“…To compare these categories we used the between-class homogeneity statistic Q to test whether at least one of the true effect sizes differed from the rest. Q has approximately a c 2 distribution (k ÿ 1 degrees of freedom, k being the number of categories) and an associated P value (Hedges & Olkin 1985;Rosenthal 1991;Rosenberg et al 1997;Archer et al 1998;Roberts et al 2004). The greater the observed value of Q, the greater was the heterogeneity of d among comparisons.…”

Section: Meta-analysesmentioning

confidence: 99%

“…Meta-analysis is a quantitative approach to summarize a body of research by examining the magnitude and the generality of a predicted pattern, while taking sample sizes into account. It also provides a way to investigate the heterogeneity among studies, and to identify modulatory variables that may account for such heterogeneity (Hedges & Olkin 1985;Rosenthal 1991;Møller & Ninni 1998;Roberts et al 2004). We analysed the existing literature on male androgen patterns in response to sexual and paternal behaviour across all vertebrates.…”

mentioning

confidence: 99%

Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis

Hirschenhauser¹,

Oliveira²

2006

Animal Behaviour

373

227

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The challenge hypothesis (Wingfield et al. 1990, American Naturalist, 136, 829-846) predicts varying androgen responses to mating, breeding or territorial behaviour in avian males. At the interspecific level, the highest androgen responsiveness has been observed in males from monogamous species with paternal incubation, and the lowest in males from promiscuous, nonpaternal species. Studies of a number of vertebrate species have discussed the extension of the challenge hypothesis predictions to nonavian vertebrates, but a general 'vertebrate consensus' has not been achieved. For this quantitative review we included data from all vertebrate species available in the literature into several meta-analyses. We distinguished between the effects of androgens on sexual, aggressive and paternal behaviour and the effects of behaviour on androgen levels and compared these effects between taxa, mating systems and types of parental care. We observed large variations between taxa in all data sets. Nevertheless, at the vertebrate level the challenge hypothesis predictions originating from the avian literature were confirmed for the modulation of androgen responsiveness (1) to sexual behaviour by paternal care but not by mating system, and (2) to paternal behaviour by mating system but not the degree of paternal care. In contrast, our results provide (3) no support for the predicted modulation of androgen levels in response to agonistic interactions by mating and parental care system at the vertebrate level. Furthermore, our meta-analyses suggest that the effects of exogenous testosterone on sexual and agonistic behaviour, as a rule of thumb, may be expected to be larger in nonpaternal than in paternal systems.

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“…Finally, testosterone may suppress immune function (Greives et al, 2006;Martin et al, 2008), either directly or indirectly by influencing the secretion of other hormones (Owen-Ashley et al, 2004;Poiani et al, 2000). This immunosuppressive effect, albeit not universal (Wingfield et al, 2001;Roberts et al, 2004), has led many to regard testosterone as a key mechanism underlying the trade-off between reproductive effort and survival (Folstad and Karter, 1992;Sheldon and Verhulst, 1996;Zera and Harshman, 2001;Hau, 2007).…”

Section: Introductionmentioning

confidence: 99%

Seasonal and population variation in male testosterone levels in breeding orange-crowned warblers (Vermivora celata)

Horton

Yoon

Ghalambor

et al. 2010

General and Comparative Endocrinology

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Testing the immunocompetence handicap hypothesis: a review of the evidence

Cited by 607 publications

References 98 publications

Effects of early developmental conditions on innate immunity are only evident under favourable adult conditions in zebra finches

Effects of early developmental conditions on innate immunity are only evident under favourable adult conditions in zebra finches

Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis

Seasonal and population variation in male testosterone levels in breeding orange-crowned warblers (Vermivora celata)

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