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: 4.45). 10/2008; 172(3):E99-112. DOI: 10.1086/589521
Source: PubMed

ABSTRACT 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.


Available from: Katrina G Salvante, Jun 16, 2015
  • [Show abstract] [Hide abstract]
    ABSTRACT: A major component of sex-allocation theory, the Trivers-Willard Model (TWM), posits that sons and daughters are differentially affected by variation in the rearing environment. In many species, the amount of parental care received is expected to have differing effects on the fitness of males and females. When this occurs, the TWM predicts that selection should favour adjustment of the offspring sex ratio in relation to the expected fitness return from offspring. However, evidence for sex-by-environment effects is mixed and little is known about the adaptive significance of producing either sex.Here, we test whether offspring sex ratios vary according to predictions of the TWM in the house wren (Troglodytes aedon, Vieillot). We also test the assumption of a sex-by-environment effect on offspring using two experiments, one in which we manipulated age-differences among nestlings within broods, and another in which we held nestling age constant but manipulated brood size.As predicted, females with high investment ability over-produced sons relative to those with lower ability. Males were also over-produced early within breeding seasons. In our experiments, the body mass of sons was more strongly affected by the sibling-competitive environment and resource availability than that of daughters: males grew heavier than females when reared in good conditions but were lighter than females when in poor conditions.Parents rearing broods with 1:1 sex ratios were more productive than parents rearing broods biased more strongly towards sons or daughters, suggesting that selection favours the production of mixed-sex broods. However, differences in the condition of offspring as neonates persisted to adulthood, and their reproductive success as adults varied with the body mass of sons, but not daughters, prior to independence from parental care. Thus, selection should favour slight but predictable variations in the sex ratio in relation to the quality of offspring that parents are able to produce.Offspring sex interacts with the neonatal environment to influence offspring fitness, thus favouring sex-ratio adjustment by parents. However, increased sensitivity of males to environmental conditions, such as sibling rivalry and resource availability, reduces the fitness returns from highly male-biased broods.This article is protected by copyright. All rights reserved.
    Journal of Animal Ecology 09/2014; 84(2). DOI:10.1111/1365-2656.12294 · 4.73 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: 1. 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. 2. 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. 3. 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. 4. 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. 5. 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. 6. 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 · 4.86 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: The immunological variation in wild populations and its relation to life-history traits has recently become a central topic in the field of evolutionary biology, considering the critical contribution of immunity to an individual's fitness. A common technique used by ecologists to estimate immunocompetence in wild populations is the phytohemagglutinin (PHA) - skin test. In this test, the degree of local swelling triggered by PHA is usually considered an estimate of T-lymphocyte activity, although there is an ongoing debate regarding this interpretation. Here, we coupled the PHA-skin test with a histological analysis to examine the temporal development of the cell-mediated response in the subterranean rodent Talas tuco-tuco (Ctenomys talarum Thomas, 1898). The inflammation response involved lymphocytes, neutrophils, eosinophils, and macrophages at the site of injection, achieving an increase of total leukocytes from 12 to 48 h after injection. However, the abundance of any of the leukocytes observed did not correlate with the degree of swelling at any time studied, suggesting that caution should be taken when interpreting the results of the PHA-induced swelling response. Particularly, the magnitude of macroscopic swelling should not be considered a priori as indicative of T-lymphocyte activity in wild-caught rodents. Our results highlight the importance of avoiding oversimplified approaches to measuring immunocompetence.
    Canadian Journal of Zoology 05/2014; 92(8):689-697. DOI:10.1139/cjz-2013-0306 · 1.35 Impact Factor