Sex‐Specific Variability in the Immune System across Life‐History Stages

Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada.
The American Naturalist (Impact Factor: 3.83). 10/2008; 172(3):E99-112. DOI: 10.1086/589521
Source: PubMed


Organisms theoretically manage their immune systems optimally across their life spans to maximize fitness. However, we lack information on (1) how the immune system is managed across life-history stages, (2) whether the sexes manage immunity differentially, and (3) whether immunity is repeatable within an individual. We present a within-individual, repeated-measures experiment examining life-history stage variation in the inflammatory immune response in the zebra finch (Taeniopygia guttata). In juveniles, age-dependent variation in immune response differed in a sex- and context-specific manner, resulting in no repeatability across stages. In adults, females displayed little stage-dependent variation in immune response when laying while receiving a high-quality (HQ) diet; however, laying while receiving a low-quality (LQ) diet significantly reduced both immune responses and reproductive outputs in a manner consistent with a facultative (resource-driven) effect of reproduction on immunity. Moreover, a reduced immune response in females who were raising offspring while receiving an HQ diet suggests a residual effect of the energetic costs of reproduction. Conversely, adult males displayed no variation in immune responses across stages, with high repeatability from the nonbreeding stage to the egg-laying stage, regardless of diet quality (HQ diet, r = 0.51; LQ diet, r = 0.42). Females displayed high repeatability when laying while receiving the HQ diet (r = 0.53); however, repeatability disappeared when individuals received the LQ diet. High-response females receiving the HQ diet had greater immune flexibility than did low-response females who were laying while receiving the LQ diet. Data are consistent with immunity being a highly plastic trait that is sex-specifically modulated in a context-dependent manner and suggest that immunity at one stage may provide limited information about immunity at future stages.

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    • "As we have confirmed that a significant reduction in immune responses occurs during incubation, the individual effects of even slightly lower levels of innate immunity could be magnified at future life history stages with serious potential repercussions on survival during a novel disease outbreak. This study highlights possible physiological trade-offs between self-maintenance and reproduction, further suggesting that links between immunocompetence and fitness are highly complex, making them difficult to document and disentangle in free-living systems (Linden and Møller 1989; Gustafsson et al. 1996; Love et al. 2008). "
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    ABSTRACT: In natural populations, epidemics provide opportunities to look for intense natural selection on genes coding for life history and immune or other physiological traits. If the populations being considered are of management or conservation concern, then identifying the traits under selection (or ‘markers’) might provide insights into possible intervention strategies during epidemics. We assessed potential for selection on multiple immune and life history traits of Arctic breeding common eiders (Somateria mollissima) during annual avian cholera outbreaks (summers of 2006, 2007 & 2008). We measured prelaying body condition, immune traits, and subsequent reproductive investment (i.e., clutch size) and survival of female common eiders and whether they were infected with Pasteurella multocida, the causative agent of avian cholera. We found no clear and consistent evidence of directional selection on immune traits; however, infected birds had higher levels of haptoglobin than uninfected birds. Also, females that laid larger clutches had slightly lower immune responses during the prelaying period reflecting possible downregulation of the immune system to support higher costs of reproduction. This supports a recent study indicating that birds investing in larger clutches were more likely to die from avian cholera and points to a possible management option to maximize female survival during outbreaks.
    Evolutionary Applications 06/2014; 7(7). DOI:10.1111/eva.12180 · 3.90 Impact Factor
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    • "These factors can interact with each other and provide the physiological framework on which phenotypic variation is based (e.g. Love et al. 2008; Henriksen, Rettenbacher & Groothuis 2011; Cohen et al. 2012). Genetic variation provides the raw material for selection and partly determines the evolutionary potential of a species . "
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    ABSTRACT: Genetic background, prenatal and post-natal early-life conditions influence the development of interconnected physiological systems and thereby shape the phenotype. Certain combinations of genotypes and pre- and post-natal conditions may provide higher fitness in a specific environmental context. Here, we investigated how grey partridges Perdix perdix of two strains (wild and domesticated) cope physiologically with pre- and post-natal predictable vs. unpredictable food supply. Food unpredictability occurs frequently in wild environments and requires physiological and behavioural adjustments. Well-orchestrated and efficient physiological systems are presumably more vital in a wild environment as compared to captivity. We thus predicted that wild-strain grey partridges have a stronger immunity, glucocorticoid (GC) stress response and oxidative stress resistance (OSR) than domesticated birds, which have undergone adaptations to captivity. We also predicted that wild-strain birds react more strongly to environmental stimuli and, when faced with harsh prenatal conditions, are better able to prepare their offspring for similarly poor post-natal conditions than birds of domesticated origin. We found that wild-strain offspring were physiologically better prepared for stressful situations as compared to the domesticated strain. They had a high GC stress response and a high OSR when kept under predictable food supply. Wild-strain parents reacted to prenatal unpredictable food supply by lowering their offspring's GC stress response, which potentially lowered GC-induced oxidative pressure. No such pattern was evident in the domesticated birds. Irrespective of strain and prenatal feeding scheme, post-natal unpredictable food supply boosted immune indices, and GC stress response was negatively related to antibody response in females and to mitochondrial superoxide production. Wild-strain grey partridge showed fitness-relevant physiological advantages and appeared to prepare their offspring for the prospective environment. Negative relationships between GC stress response, immunity and oxidative indices imply a pivotal role of an organism's oxidative balance and support the importance of considering multiple physiological systems simultaneously.
    Functional Ecology 08/2013; 27(4):1042-1054. DOI:10.2307/23481011 · 4.83 Impact Factor
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    • "Early developmental conditions can further be expected to differentially affect adult innate immunity in male and female zebra finches, as the latter have been shown to be more negatively affected by harsh rearing conditions (e.g. Bradbury and Blakey 1998; de Kogel 1997b; Kilner 1998; Martins 2004; Verhulst et al. 2006), and inflammatory and humoral immune responses have been shown to vary between sexes and contexts (Love et al. 2008; McGraw and Ardia 2005). Furthermore, increased foraging costs in adulthood result in physiological adjustments to save energy (Wiersma et al. 2005; Wiersma and Verhulst 2005) and might therefore also affect innate immunity because of the associated energetic costs (Klasing 2004). "
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    The Science of Nature 11/2011; 98(12):1049-56. DOI:10.1007/s00114-011-0863-3 · 2.10 Impact Factor
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