Early-Life Stress Has Sex-Specific Effects on Immune Function in Adult Song Sparrows

Schmidt, Kim L.; Kubli, Shawn P.; MacDougall‐Shackleton, Elizabeth A.; MacDougall‐Shackleton, Scott A.

doi:10.1086/680599

Cited by 14 publications

(17 citation statements)

References 50 publications

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“…Alternatively, males may suffer the same damage from CORT as females but may invest differently in repair, e.g. by prioritizing investment into sexual traits over investment into antioxidant or immune defences (Schmidt, Kubli, MacDougall-Shackleton, & MacDougall-Shackleton, 2015). Finally, high stress reactivity can also be related to the social status of the individual (Creel, Dantzer, Goymann, & Rubenstein, 2013;Rubenstein, 2007), or to differences in behavioural responses or personality traits (e.g.…”

Section: Discussionmentioning

confidence: 99%

Male but not female zebra finches with high plasma corticosterone have lower survival

et al. 2017

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The glucocorticoid axis is essential for coping with predictable and unpredictable environmental variation. Despite this vital function, attempts to link individual variation in the glucocorticoid axis to survival have yielded mixed results, which may be due to endocrine variation caused by uncontrolled variation in environment and life‐history traits such as reproductive effort. We therefore studied the link between the glucocorticoid axis and long‐term survival using captive non‐breeding zebra finches. We quantified the relationship between survival over a three‐year period and plasma corticosterone concentrations: (1) baseline, (2) stress‐induced, (3) after induction of negative feedback via dexamethasone injection and (4) after maximal adrenal stimulation via adrenocorticotropin hormone injection. Only stress‐induced corticosterone predicted survival, with higher concentrations being associated with lower survival. However, this effect differed significantly between the sexes, being present only in males. Stress‐induced corticosterone concentration is the sum of baseline corticosterone and the corticosterone increase in response to the standardized stressor, and both components were similarly associated with male survival in a model that included both variables. This implies that baseline corticosterone itself also exerts an effect on male survival, but this was only revealed when the stress‐induced corticosterone increase was included in the model, presumably because this increased statistical power. Given that corticosterone concentrations are highly repeatable in our study population and independent of manipulated foraging conditions, these data suggest that endocrine stress reactivity may be a major component determining male life span, presumably also in wild populations. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13021/suppinfo is available for this article.

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Section: Discussionmentioning

confidence: 99%

Male but not female zebra finches with high plasma corticosterone have lower survival

et al. 2017

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“…before sexual maturity) can experience sustained immunosuppressive consequences in adulthood (e.g. Michaut et al, 1981;Avitsur et al, 2006;Schmidt et al, 2015). To verify whether early-life stress can program the immune response, direct manipulation of glucocorticoids and environmentally relevant stressors in early life is necessary (Grindstaff and Merrill, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Michaut et al, 1981;Avitsur et al, 2006) and birds (e.g. De Coster et al, 2011;Kriengwatana et al, 2013;Schmidt et al, 2015;Grindstaff and Merrill, 2017), with less known about lasting effects of early-life stress on immune function in ectotherms. Ectotherms are unable to internally regulate temperature and may allocate resources toward the immune system in a different manner from ectotherms (Zimmerman et al, 2010); thus, ectotherms may experience different immune consequences of early-life stress compared to endotherms.…”

Section: Introductionmentioning

confidence: 99%

Population history with invasive predators predicts innate immune function response to early life glucocorticoid exposure

McCormick

Robbins

Cavigelli

et al. 2019

Journal of Experimental Biology

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Early-life stress can suppress immune function, but it is unclear whether transgenerational stress exposure modulates the immune consequences of early stress. In populations where, historically, the immune system is frequently activated, e.g. persistent stressors that cause injury, it may be maladaptive to suppress immune function after early-life stress. Thus, the relationship between early-life stress and immune function may vary with population-level historical stressor exposure. We collected gravid fence lizards (Sceloporus undulatus) from populations that naturally differ in long-term exposure to invasive fire ants (Solenopsis invicta). We manipulated early-life stress in the resulting offspring via weekly exposure to fire ants, application of the stress-relevant hormone corticosterone or control treatment from 2 to 43 weeks of age. We quantified adult immune function in these offspring with baseline and antigen-induced hemagglutination and plasma bacterial killing ability. Early-life corticosterone exposure suppressed baseline hemagglutination in offspring of lizards from populations not exposed to fire ants but enhanced hemagglutination in those from populations that were exposed to fire ants. This enhancement may prepare lizards for high rates of wounding, toxin exposure and infection associated with fire ant attack. Adult bacterial killing ability and hemagglutination were not affected by early-life exposure to fire ants, but the latter was higher in offspring of lizards from invaded sites. A population's history of persistent stress may thus alter individual long-term immunological responses to early-life stressors. Further consideration of historical stressor exposure (type and duration) may be important to better understand how early-life stressors affect adult physiology.

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“…A number of studies have demonstrated that exposure to stressors or exogenous glucocorticoids during early postnatal life can impact immune responses over the short term (e.g., Loiseau, Sorci, Dano, & Chastel, ; Saino, Suffritti, Martinelli, & Møller, ; Schoech, Rensel, & Heiss, ; Stier et al., ). However, few studies have tested for persistent effects of developmental exposure to glucocorticoids or stress on adult immune function, especially in nonmammalian model systems (Schmidt, Kubli, MacDougall‐Shackleton, & MacDougall‐Shackleton, ). Finally, previous studies have generally not tested for interactions between developmental and adult environmental conditions on adult immune responses (e.g., De Coster et al., ).…”

Section: Introductionmentioning

confidence: 99%

Developmental corticosterone treatment does not program immune responses in zebra finches (Taeniopygia guttata)

Grindstaff

Merrill

2017

J Exp Zool Pt A

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Developmental conditions may impact the expression of immune traits throughout an individual’s life. Early-life challenges may lead to immunological constraints that are mediated by endocrine-immune interactions. In particular, individual differences in the ability to mount immune responses may be programmed by exposure to stressors or glucocorticoid hormones during development. To test this hypothesis, we experimentally elevated levels of the glucocorticoid hormone corticosterone during the nestling and fledgling periods in captive zebra finches (Taeniopygia guttata). We subsequently challenged birds with the antigen lipopolysaccharide (LPS) on days 60 and 100 post-hatch to determine if developmental exposure to elevated corticosterone impacted the later response to LPS. As measures of immune function, we quantified bacteria killing ability, haptoglobin concentrations, and LPS-specific antibody responses at multiple time points. We also measured circulating corticosterone concentrations during the experimental period and on day 60 before and after endotoxin challenge. During the experimental period, corticosterone treatment elevated corticosterone levels. Corticosterone treatment did not induce programming effects on immune function or corticosterone production. Independent of treatment, individuals with higher corticosterone concentrations during the nestling period had lower bacteria killing ability on day 36 and higher baseline corticosterone concentrations on day 60 post-hatch. These results suggest a limited role for corticosterone exposure during early life to mediate immunological constraints later in life. Manipulation of cortisol may be necessary to conclusively determine if developmental glucocorticoid exposure can program immune function in birds. To determine if developmental stress can program the immune response, exposure to environmentally relevant stressors should also be manipulated.

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Early-Life Stress Has Sex-Specific Effects on Immune Function in Adult Song Sparrows

Cited by 14 publications

References 50 publications

Male but not female zebra finches with high plasma corticosterone have lower survival

Male but not female zebra finches with high plasma corticosterone have lower survival

Population history with invasive predators predicts innate immune function response to early life glucocorticoid exposure

Developmental corticosterone treatment does not program immune responses in zebra finches (Taeniopygia guttata)

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