Developmental immune activation programs adult behavior: insight from research on birds

Grindstaff, Jennifer L.

doi:10.1016/j.cobeha.2015.10.006

Cited by 17 publications

(21 citation statements)

References 56 publications

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“…This is surprising given that previous studies have documented significant increases in Hp after immune challenge, particularly with LPS (Millet, Bennett, Lee, Hau, & Klasing, ; Van de Crommenacker et al., ). Nonetheless, the negative associations between Hp levels during development and song phrases and song duration in adulthood indicate that exposure to inflammation or oxidative stress may influence aspects of adult song production (Grindstaff, ), although this would have to be verified via experimental manipulation during development.…”

Section: Discussionmentioning

confidence: 99%

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Early‐life immune activation increases song complexity and alters phenotypic associations between sexual ornaments

et al. 2017

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Summary Early-life adversity can have long-lasting effects on physiological, behavioural, cognitive, and somatic processes. Consequently, these effects may alter an organism’s life-history strategy and reproductive tactics.In response to early-life immune activation, we quantified levels of the acute phase protein haptoglobin (Hp) during development in male zebra finches (Taeniopygia guttata). Then, we examined the long-term impacts of early-life immune activation on an important static sexual signal, song complexity, as well as effects of early-life immune activation on the relationship between song complexity and a dynamic sexual signal, beak colouration. Finally, we performed mate-choice trials to determine if male early-life experience impacted female preference.Challenge with keyhole limpet hemocyanin (KLH) resulted in increased song complexity compared to lipopolysaccharide (LPS) treatment or the control. Hp levels were inversely correlated with song complexity. Moreover, KLH-treatment resulted in negative associations between the two sexual signals (beak colouration and song complexity). Females demonstrated some preference for KLH-treated males over controls and for control males over LPS-treated males in mate choice trials.Developmental immune activation has variable effects on the expression of secondary sexual traits in adulthood, including enhancing the expression of some traits. Because developmental levels of Hp and adult song complexity were correlated, future studies should explore a potential role for exposure to inflammation during development on song learning.Early-life adversity may differentially impact static versus dynamic signals. The use of phenotypic correlations can be a powerful tool for examining the impact of early-life experience on the associations among different traits, including sexual signals.

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Section: Discussionmentioning

confidence: 99%

“…Nonetheless, the negative associations between Hp levels during development and song phrases and song duration in adulthood indicate that exposure to inflammation or oxidative stress may influence aspects of adult song production (Grindstaff, 2016), although this would have to be verified via experimental manipulation during development.…”

Section: Discussionmentioning

confidence: 99%

Early‐life immune activation increases song complexity and alters phenotypic associations between sexual ornaments

et al. 2017

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“…Conversely, stimulation of the NEI circuit by infection or immunogens can produce stereotypical and adaptive changes in behavior that are collectively termed sickness behavior (discussed below). In addition, maternal immune challenge can also affect personality of offspring and predisposition to disease (Butler et al, 2012; Grindstaff, 2016; Khan et al., 2014). Thus, behavior affects NEI interactions and vice versa (Fig.…”

Section: Nei Circuits and Behaviormentioning

confidence: 99%

Neuroendocrine-immune circuits, phenotypes, and interactions

Ashley

Demas

2017

Hormones and Behavior

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Multidirectional interactions among the immune, endocrine, and nervous systems have been demonstrated in humans and non-human animal models for many decades by the biomedical community, but ecological and evolutionary perspectives are lacking. Neuroendocrine-immune interactions can be conceptualized using a series of feedback loops, which culminate into distinct neuroendocrine-immune phenotypes. Behavior can exert profound influences on these phenotypes, which can in turn reciprocally modulate behavior. For example, the behavioral aspects of reproduction, including courtship, aggression, mate selection and parental behaviors can impinge upon neuroendocrine-immune interactions. One classic example is the immunocompetence handicap hypothesis (ICHH), which proposes that steroid hormones act as mediators of traits important for female choice while suppressing the immune system. Reciprocally, neuroendocrine-immune pathways can promote the development of altered behavioral states, such as sickness behavior. Understanding the energetic signals that mediate neuroendocrine-immune crosstalk is an active area of research. Although the field of psychoneuroimmunology (PNI) has begun to explore this crosstalk from a biomedical standpoint, the neuroendocrine-immune-behavior nexus has been relatively underappreciated in comparative species. The field of ecoimmunology, while traditionally emphasizing the study of non-model systems from an ecological evolutionary perspective, often under natural conditions, has focused less on the physiological mechanisms underlying behavioral responses. This review summarizes neuroendocrine-immune interactions using a comparative framework to understand the ecological and evolutionary forces that shape these complex physiological interactions.

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“…Negative correlations between corticosterone levels and body condition or habitat quality are consistent with this hypothesis (Jenni‐Eiermann et al., ; Müller et al., ), as are reports of negative effects of maternally derived corticosterone on nestling growth and development (Henriksen et al., ; Schoech et al., ). In contrast to this traditional view, an emerging body of empirical research suggests that maternal effects can be a powerful tool by which mothers shape the phenotype of their offspring so that they are optimally suited to the environment in which they develop, the environmental‐/maternal‐matching hypothesis (Crino & Breuner, ; Grindstaff, ; Henriksen et al., ; Merrill & Grindstaff, ; Sheriff & Love, ; Sheriff et al., ). This hypothesis posits a positive relationship between an increase in maternally derived corticosterone and offspring fitness, particularly if the corticosterone that females transfer to their offspring via the egg prepares offspring for success under the stressful conditions that their mother experienced (Chin et al., ; Groothuis, Müller, von Engelhardt, Carere, & Eising, ).…”

Section: Introductionmentioning

confidence: 99%

Pre‐ and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens

et al. 2018

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Corticosterone plays a central role in maintaining homeostasis, promoting energy acquisition, and regulating the stress response in birds. Exposure to elevated levels of corticosterone during development can profoundly alter offspring behaviour and physiology, but the effects of elevated maternal corticosterone on offspring development remain poorly understood.We tested two competing hypotheses concerning the effect of maternally derived corticosterone on growth and development of free-living house wrens: (i) elevated maternal corticosterone causes damaging effects on nestling phenotype and fitness (collateral damage hypothesis) and (ii) increased maternal corticosterone enhances offspring fitness by preparing nestlings for the environment experienced by their mother (environmental/maternal-matching hypothesis).We used a non-invasive means to increase maternal corticosterone by providing females with corticosterone-injected mealworms prior to and during egg production in the absence of any overt pre-natal maternal stress. To disentangle pre- and post-natal effects of this elevation in maternal corticosterone, we cross-fostered young in two experiments: (i) nestlings of control and experimental females were reared by unmanipulated, natural females in a uniform maternal environment; (ii) a split-brood design that enabled us to assess the interaction between the mother’s corticosterone treatment and that of the nestlings.There were significant pre-natal effects of increased maternal corticosterone on nestling growth and survival. Offspring of females experiencing experimentally increased corticosterone were heavier and larger than offspring of control females. There also was a significant interaction between maternal corticosterone treatment and the corticosterone treatment to which young were exposed within the egg in their effect on nestling survival while in the nest; experimental young exhibited greater survival than control young, but only when reared by control mothers. There was also a significant effect of maternal corticosterone treatment on nestling stress reactivity and, in both experiments, on the eventual recruitment of offspring as breeding adults in the local population.These patterns are broadly consistent with the environmental/maternal-matching hypothesis, and highlight the importance of disentangling pre- and post-natal effects of manipulations of maternal hormone levels on offspring phenotype.

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Developmental immune activation programs adult behavior: insight from research on birds

Cited by 17 publications

References 56 publications

Early‐life immune activation increases song complexity and alters phenotypic associations between sexual ornaments

Early‐life immune activation increases song complexity and alters phenotypic associations between sexual ornaments

Neuroendocrine-immune circuits, phenotypes, and interactions

Pre‐ and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens

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