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

Coster, Greet De; Verhulst, Simon; Koetsier, Egbert; Neve, Liesbeth De; Briga, Michael; Lens, Luc

doi:10.1007/s00114-011-0863-3

Cited by 26 publications

(24 citation statements)

References 56 publications

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“…Therefore, early-life CORT treatment appears to affect some components of the innate immune system in song sparrows, such as the activity of phagocytes, but not others, such as the complement system. In contrast, adult zebra finches reared in experimentally enlarged broods exhibited decreased lysis of rabbit erythrocytes when housed in favorable adult conditions (De Coster et al 2011). The fact that lysis of rabbit erythrocytes is primarily mediated by interactions between complement proteins and natural antibodies (Millet et al 2007) suggests that variation in the early-rearing environment did have long-term effects on complement proteins and natural antibodies.…”

Section: Constitutive Innate Immune Functionmentioning

confidence: 99%

“…However, very few studies have investigated the long-term effects of early-life stress on immunity in nonmammalian species. In one study, zebra finches (Taeniopygia guttata) reared in experimentally enlarged broods had suppressed innate immunity compared to individuals reared in small broods, when tested under favorable adult conditions (De Coster et al 2011). Also in zebra finches, individuals subjected to nutritional stress as juveniles had higher antimicrobial activity toward a strain of Candida albicans compared to individuals that did not experience juvenile nutritional stress (Kriengwatana et al 2013).…”

Section: Introductionmentioning

confidence: 99%

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

Schmidt

Kubli²,

MacDougall‐Shackleton³

et al. 2015

Physiological and Biochemical Zoology

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Multiple components of the immune system are modulated by environmental factors, including exposure to stressors. In particular, chronic stressors can impair development of the immune system, leading to alterations in immune function in adulthood. While these effects have been well established in mammals, less is known about how developmental stress modulates immunity in nonmammalian species. We determined the long-term effects of exposure to early-life stressors on immunity in song sparrows including the swelling response to phytohemagglutinin (PHA) and several measures of constitutive innate immunity. Song sparrows were reared in captivity from 3 d of age and exposed to control conditions, food restriction, or corticosterone (CORT) treatment. Males exposed to food restriction or CORT treatment had less swelling of the wing web in response to PHA than control males; however, neither treatment affected the swelling response to PHA in females. The treatments also had sex-specific effects on constitutive innate immune function. Specifically, CORT-treated males had lower antimicrobial capacity toward a strain of the bacterium E. coli but higher antimicrobial activity toward a strain of the fungus Candida albicans compared to food-restricted or control males. In contrast, neither treatment affected constitutive innate immunity in females. These results suggest that male and female song sparrows may differ in how they allocate resources to development of the immune system when reared in stressful or food-limited conditions.

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Section: Constitutive Innate Immune Functionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Schmidt

Kubli²,

MacDougall‐Shackleton³

et al. 2015

Physiological and Biochemical Zoology

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“…We used 125 Zebra Finches (66 females; 57 males), originating from 73 broods, reared from stock that were part of a long-term experiment, in which natal brood size and energy expenditure required for foraging were manipulated (De Coster et al 2011;Koetsier and Verhulst 2011). With respect to the foraging cost manipulation, we only used control birds that had easy access to food.…”

Section: Study Species and Samplingmentioning

confidence: 99%

Heritability of telomere length in the Zebra Finch

et al. 2015

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Telomere length predicts survival in birds, and many stressors that presumably reduce fitness have also been linked to telomere length. The response to selection of telomere length will be largely determined by the heritability of this trait; however, little is known about the genetic component of telomere length variation in animals other than humans. Moreover, published heritability estimates of telomere length are based on telomere measurements with techniques that do not distinguish between terminal telomeres, which are susceptible to age and stress, and the interstitial telomeric repeats, which are relatively inert. Heritability estimates that combine interstitial and terminal telomeres are difficult to interpret in species such as birds, where interstitial telomeres are often numerous. We estimated the heritability of terminal telomere length in a captive Zebra Finch population of cross-fostered (half-)siblings using data obtained with an electrophoresis technique that excludes the interstitial repeats from the measurements. We used both a Bayesian quantitative genetic 'animal' model and a frequentist sibling regression approach to estimate heritability. With the animal model, we estimated a high heritability of telomere length (h 2 = 0.99, 95 % credible interval = 0.87-1), but had insufficient statistical power to separate parental and permanent environment effects. The frequentist approach yielded similar heritability estimates, although with large confidence intervals. We used general linear mixed models to disentangle variance components of telomere length. The relative contributions of the individual, mother and father to telomere length variation were statistically indistinguishable at 23-31 %. Chicks were cross-fostered 4-days after hatching, and no effect of rearing nest was found, indicating that any undetected environmental effects exerted their influence prior to, or soon after, hatching. Thus, we conclude that telomere length resemblance between relatives is high and proportional to their relatedness, but we cannot conclusively distinguish between genetic and other forms of inheritance.

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“…Thus it is not surprising that agglutination titres did not differ between groups 13h post challenge. The increase in lysis titres during infection points to another important topic of ecoimmunology: high values are not necessarily better (De Coster et al, 2011). Instead, values should be viewed in relation to the immunological status, e.g.…”

Section: Physiological Responses After Immune Challengementioning

confidence: 99%

Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird

Hegemann

Matson

Versteegh

et al. 2013

Journal of Experimental Biology

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SUMMARYTrade-offs between immune function and other physiological and behavioural processes are central in ecoimmunology, but one important problem is how to distinguish a reallocation of resources away from the immune system from a reallocation or redistribution within the immune system. While variation in baseline values of individual immune parameters is well established, studies in wild animals on multiple parameters during an immune response are lacking. It also remains to be tested whether and how immune responses correlate with baseline values that vary, for example, over the course of an annual cycle. We studied immunological responses to an endotoxin challenge in skylarks (Alauda arvensis), a partial migrant bird breeding in temperate zones. We compared birds injected with the endotoxin LPS with un-injected controls, characterizing immunological responses with leukocyte profiles, titres of lytic enzymes and natural antibodies, and concentrations of haptoglobin and heat shock proteins. We did this in five annual-cycle stages to test whether the response varied throughout the year. The endotoxin challenge affected six of 10 measured parameters. Lysis titres and proportions of heterophils increased; haptoglobin concentrations and proportions of lymphocytes, basophils and eosinophils decreased. The variable effects on different immune components demonstrate the complexity of an immune response. We found no evidence that the response differed between annual-cycle stages. The response was independent of baseline measures taken directly upon capture in the field, indicating that birds were facing no immunological ceiling when mounting an immune response. Values of five parameters collected under field conditions were significantly related to values taken under standardized laboratory conditions. We conclude that multiple parts of the immune system are modulated during an immunological response and that responses are not re-organized throughout the annual cycle.Key words: inflammation, ecological immunology, acute phase response, lipopolysaccharide, LPS, annual cycle, birds. Received 20 November 2012; Accepted 8 March 2013The Journal of Experimental Biology 216, 2573Biology 216, -2580Biology 216, © 2013 Nelson, 2004;Hasselquist, 2007;Martin et al., 2008). Immunological mechanisms aimed at avoiding autoimmunity (Råberg et al., 1998) and preventing oxidative stress (Sorci and Faivre, 2009) might further influence this process. Several studies on non-induced (baseline) immune function indeed show that different indices express different seasonal patterns among and within annual-cycle stages (Nelson and Demas, 1996;Buehler et al., 2008b;Pap et al., 2010a;Pap et al., 2010b;Hegemann et al., 2012c). Thus, reorganization of baseline immune function appears to depend on both environmental conditions and competing biotic processes. Data on seasonal variation in induced immune responses are scarce. However, these are the data needed to verify the hypothesis that free-living birds switch from costly inflammatory respo...

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

Cited by 26 publications

References 56 publications

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

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

Heritability of telomere length in the Zebra Finch

Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird

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