Androgens and the Immunocompetence Handicap Hypothesis: Unraveling Direct and Indirect Pathways of Immunosuppression in Song Sparrows

Owen-Ashley, Noah T; Hasselquist, Dennis; Wingfield, John C.

doi:10.1086/423714

Cited by 202 publications

(112 citation statements)

References 97 publications

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“…During September 2004 and September 2005, we measured humoral immunity as a song sparrow's primary antibody response to tetanus and diphtheria toxoids (Hasselquist et al . 1999, 2001; Owen-Ashley et al . 2004).…”

Section: Methodsmentioning

confidence: 99%

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Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

et al. 2006

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The consequences of inbreeding for host immunity to parasitic infection have broad implications for the evolutionary and dynamical impacts of parasites on populations where inbreeding occurs. To rigorously assess the magnitude and the prevalence of inbreeding effects on immunity, multiple components of host immune response should be related to inbreeding coefficient ( f ) in free-living individuals. We used a pedigreed, free-living population of song sparrows (Melospiza melodia) to test whether individual responses to widely used experimental immune challenges varied consistently with f. The patagial swelling response to phytohaemagglutinin declined markedly with f in both females and males in both 2002 and 2003, although overall inbreeding depression was greater in males. The primary antibody response to tetanus toxoid declined with f in females but not in males in both 2004 and 2005. Primary antibody responses to diphtheria toxoid were low but tended to decline with f in 2004. Overall inbreeding depression did not solely reflect particularly strong immune responses in outbred offspring of immigrant-native pairings or weak responses in highly inbred individuals. These data indicate substantial and apparently sex-specific inbreeding effects on immune response, implying that inbred hosts may be relatively susceptible to parasitic infection to differing degrees in males and females.

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Section: Methodsmentioning

confidence: 99%

“…Primary antibody responses peak 9–15 days after vaccination in song sparrows and other passerines (Hasselquist et al . 1999; Owen-Ashley et al . 2004).…”

Section: Methodsmentioning

confidence: 99%

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

et al. 2006

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“…One possible mechanism for a behavioral alteration due to the presence of a female would be through changes in circulating testosterone. Several lines of evidence suggest that testosterone can have immunosuppressive effects in both mammals [27,28,29,30]and birds [31,32,33,34,35,36], although there are exceptions in both taxa (mammals: [37,38,39] and no effect in birds: [40,41,42]). Social modulation of testosterone may minimize the costs associated with maintaining high levels of testosterone (e.g.…”

Section: Introductionmentioning

confidence: 99%

The Impact of Exposure to a Novel Female on Symptoms of Infection and on the Reproductive Axis

Lopes¹,

Chan²,

Demathieu³

et al. 2013

Neuroimmunomodulation

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Background/Aim: Sickness behaviors are the behavioral alterations animals exhibit during the course of an infection, often accompanied by reduced reproductive activity. Adopting sickness behaviors may aid in overcoming the infection, by diverting energy from routine activities towards enhancement of the immune system. Nonetheless, sickness behaviors are plastic, being influenced by specific environmental and social circumstances. Here, we tested whether the presentation of a novel female to males suffering from a simulated infection could impact the behavioral effects of sickness, the reproductive axis, or both. Methods: Male zebra finches were housed in isolation and injected intramuscularly with lipopolysaccharide or saline. Behaviors were recorded before (3 h before injection) and after (3.5 h after injection) addition of a novel female to the cage for 30 min. Four hours after injection, we collected the brain and testis for the analysis of important reproductive axis modulators, gonadotropin-releasing hormone, and gonadotropin-inhibitory hormone, and to quantify gene expression of a proinflammatory cytokine involved in the regulation of sickness behaviors [interleukin (IL)-1β]. Testosterone was quantified in the plasma. Results: The presence of a novel female diminished sickness behaviors and induced alterations in the reproductive axis within 30 min, with no associated changes in brain gene expression of IL-1β. Social environment itself altered brain gene expression of IL-1β. Conclusions: Male zebra finches prioritize the opportunity to mate versus investment in recovery from an infection, as determined by reduced expression of sickness behaviors when a potential mate was present. The behavioral effects of IL-1β appear to be context dependent in this species.

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“…Many mechanistic alternatives have been proposed to explain the inconsistency of the results in the literature, suggesting the presence of confounding variables or intermediate physiological pathways that would mask the impact of testosterone on immunity (Owen-Ashley et al 2004;Blas et al 2006;Alonso-Alvarez et al 2007a,b;McGraw & Ardia 2007;Kempenaers et al 2008).…”

Section: Introductionmentioning

confidence: 99%

Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling

et al. 2009

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The immunocompetence handicap hypothesis proposes that testosterone mediates a trade-off between sexual signalling and immunocompetence in males. Such a trade-off could favour the reliability of sexual signals on the basis that testosterone required for signal expression also promotes immunosuppression. However, the immunosuppressive activity of testosterone has not been convincingly demonstrated. We propose that the optimal solution to the testosterone-mediated trade-off should change with age, explaining ambiguous results in the past. Testosterone and ageing would promote two simultaneous immunosuppressive challenges unaffordable for low-quality males. Oxidative stress, as intimately related to ageing and immunosenescence, could contribute to enhance signal reliability. In this context, traits coloured by carotenoids (yellow-red traits) could play a crucial role due to the immunostimulatory and antioxidant properties of these pigments. Here, old and middle-aged male red-legged partridges were treated with testosterone or manipulated as controls. In the presence of high-testosterone levels, middleaged males increased both circulating carotenoid levels and colour expression, whereas their cell-mediated immunity was not significantly altered. However, in old males, neither circulating carotenoids nor sexual signalling increased when treated with testosterone, but immunosuppression was detected. The link between testosterone and carotenoids could favour the reliability of sexual signals throughout the life.

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Androgens and the Immunocompetence Handicap Hypothesis: Unraveling Direct and Indirect Pathways of Immunosuppression in Song Sparrows

Cited by 202 publications

References 97 publications

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

The Impact of Exposure to a Novel Female on Symptoms of Infection and on the Reproductive Axis

Testosterone-mediated trade-offs in the old age: a new approach to the immunocompetence handicap and carotenoid-based sexual signalling

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