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van Kesteren, F.

Publications and source records attributed to van Kesteren, F..

6 recordsLinked to original sources

Timing-dependent effects of elevated maternal glucocorticoids on offspring brain gene expression in a wild small mammal

An increase in maternal stress during offspring development can have cascading, life-long impacts on offspring behavior and physiology, which can vary depending on the timing of exposure to the stressor. By responding to stressors through increasing production of glucocorticoids (GCs), the hypothalamic-pituitary-adrenal (HPA) axis is a key mediator of maternal effects - both on the side of the mother and the offspring. At a molecular level, maternal effects are thought to be mediated through modifying transcription of genes, particularly in the brain. To better understand the evolutionary implications of maternal effects, more studies are needed on mechanisms of maternal effects in wild populations. To test how the timing of maternal stress impacts gene expression in the brains of offspring, we treated free-ranging North American red squirrels (Tamiasciurus hudsonicus) with GCs during late pregnancy or early lactation and collected brains from offspring around weaning. We used RNA-sequencing to measure gene expression in the hypothalamus and hippocampus. We found small differences in gene expression between GC-treated and control individuals suggesting long-term effects of the GC treatment on neural gene transcription. The general patterns of gene regulation across the transcriptome were consistent between the pregnancy and lactation-treated individuals. However, the number of significantly differentially expressed genes was higher in the lactation treatment group. These results support the idea that maternal stress affects neural gene expression in offspring, and these effects are dependent on timing. Our findings add valuable insight into the impact of maternal hormones on neural transcriptomics in a wild population.

ecology↗

Maternal glucocorticoids do not influence HPA axis activity or behavior of juvenile wild North American red squirrels

Environmental factors experienced during development can affect the physiology and behavior of offspring. Maternal glucocorticoids (GCs) may convert environmental cues experienced by the mother into a cue triggering adaptive developmental plasticity in offspring. In North American red squirrels (Tamiasciurus hudsonicus), females exhibit increases in GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under high density conditions. We experimentally elevated maternal GCs during gestation or early lactation to test the hypothesis that elevated maternal GCs cause shifts in offspring aggression and activity that may prepare them for high density conditions. When offspring were weaned, we measured two behavioral traits (activity and aggression) using a standardized behavioral assay. Because maternal GCs may influence offspring hypothalamic-pituitary-adrenal (HPA) axis activity and HPA axis activity may in turn affect offspring behavior, we also measured the impact of our treatments on offspring HPA axis activity (adrenal reactivity and negative feedback) and the association between offspring HPA axis activity and behavior. Increased maternal GCs during lactation, but not gestation, only slightly elevated activity levels in offspring. Offspring aggression, adrenal reactivity, and negative feedback did not differ between GC-treated and control groups. Offspring with higher adrenal reactivity did exhibit lower aggression, but the relationship between adrenal reactivity and aggression was not affected by treatment with maternal GCs. These results suggest maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce changes in behavioral and physiological stress responses in offspring in natural populations. Summary StatementWe found maternal glucocorticoid levels do not influence offspring personality or HPA axis dynamics in North American red squirrels. Regardless of maternal glucocorticoid treatment, more aggressive squirrels exhibited lower adrenal reactivity.

animal behavior and cognition↗

Maternal stress promotes offspring growth without oxidative costs in wild red squirrels

Elevations in glucocorticoid levels (GCs) in breeding females may induce adaptive shifts in offspring life histories. Offspring produced by mothers with elevated GCs may be better prepared to face harsh environments where a faster pace of life is beneficial. We examined how experimentally elevated GCs in pregnant or lactating North American red squirrels (Tamiasciurus hudsonicus) affected offspring postnatal growth, structural size, oxidative stress levels (two antioxidants and oxidative protein damage) in three different tissues (blood, heart, liver), and liver telomere lengths. We predicted that offspring from mothers treated with GCs would grow faster but would also have higher levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring from mothers treated with GCs during pregnancy were 8.3% lighter around birth but grew (in body mass) 17.0% faster than those from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% slower than those from controls and did not differ in body mass around birth. Treating mothers with GCs during pregnancy or lactation did not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring from any of the treatment groups did not have higher oxidative stress levels or shorter telomere lengths, indicating that offspring that grew faster early in life did not exhibit oxidative costs after this period of growth. Our results indicate that elevations in maternal GCs may induce plasticity in offspring growth without long-term oxidative costs to the offspring that might result in a shortened lifespan. Summary StatementWe show that experimental increases in glucocorticoids in breeding female North American red squirrels affects offspring postnatal growth but not levels of oxidative damage and antioxidants or telomere lengths.

evolutionary biology↗

Individual variation in phenotypic plasticity of the stress axis

Phenotypic plasticity--one individuals capacity for phenotypic variation under different environments--is critical for organisms facing fluctuating conditions within their lifetime. North American red squirrels (Tamiasciurus hudsonicus) experience drastic among-year fluctuations in conspecific density. This shapes juvenile competition over vacant territories and overwinter survival. To help young cope with competition at high densities, mothers can increase offspring growth rates via a glucocorticoid-mediated maternal effect. However, this effect is only adaptive under high densities, and faster growth often comes at a cost to longevity. While experiments have demonstrated that red squirrels can adjust hormones in response to fluctuating density, the degree to which mothers differ in their ability to regulate glucocorticoids across changing densities remains unknown--little is known about within-individual plasticity in endocrine traits relative to among-individual variation. Findings from our reaction norm approach revealed significant individual variation not only in a female red squirrels mean endocrine phenotype, but also in endocrine plasticity in response to changes in local density. Future work on the proximate and ultimate drivers of variation in the plasticity of endocrine traits and maternal effects is needed, particularly in free-living animals experiencing fluctuating environments.

zoology↗

Stress activity is not predictive of coping style in North American red squirrels

Individuals vary in their behavioral and physiological responses to environmental changes. These behavioral responses are often described as coping styles along a proactive-reactive continuum. Studies in laboratory populations often, but not always, find that behavioral responses and physiological responses to stressors covary, where more proactive (more aggressive and active) individuals have a lower physiological stress response, specifically as measured by hypothalamic-pituitary-adrenal (HPA) axis activity. These studies support the possibility of hormonal pleiotropy underlying the presentation of behaviors that make up the proactive-reactive phenotype. However, recent research in wild populations is equivocal, with some studies reporting the same pattern as found in many controlled laboratory studies, whereas others do not. We tested the hypothesis that physiological and behavioral stress responses are correlated in wild adult North American red squirrels (Tamiasciurus hudsonicus). We used fecal cortisol metabolites (FCMs) as a non-invasive, integrated estimate of circulating glucocorticoids for our measurement of HPA axis activity. We found that FCM concentrations were not correlated with three measures of behavioral coping styles (activity, aggression, and docility) among individuals. This does not support the hypothesis that hormonal pleiotropy underlies a proactive-reactive continuum of coping styles. Instead, our results support the \"two-tier\" hypothesis that behavioral and physiological stress responses are independent and uncorrelated traits among individuals in wild populations that experience naturally varying environments rather than controlled environments. If also found in other studies, this may alter our predictions about the evolutionary consequences of behavioral and endocrine coping styles in free-living animals.\n\nSignificance StatementIndividuals vary in how they respond to stressors through behavior and physiology, but we find the two responses are independent in wild animals. Many laboratory studies find links between the behavioral and physiological stress responses, however studies conducted with wild populations are less conclusive. In wild North American red squirrels, independence between the physiological response and behavioral response may allow adaptive responses to a changing environment without pleiotropic constraint.

animal behavior and cognition↗

Experimental increases in glucocorticoids alter function of the neuroendocrine stress axis in wild red squirrels without negatively impacting survival and reproduction

Hormones such as glucocorticoids (colloquially referred to as "stress hormones") have important effects on animal behavior and life history traits, yet most of this understanding has come through correlative studies. While experimental studies offer the ability to assign causality, there are important methodological concerns that are often not considered when manipulating hormones, including glucocorticoids, in wild animals. In this study, we examined how experimental elevations of cortisol concentrations in wild North American red squirrels (Tamiasciurus hudsonicus) affected their hypothalamic-pituitary-adrenal (HPA) axis reactivity, and life history traits including body mass, litter survival, and adult survival. The effects of exogenous cortisol on plasma cortisol concentrations depended on the time between treatment consumption and blood sampling. In the first nine hours after consumption of exogenous cortisol, individuals had significantly higher true baseline plasma cortisol concentrations, but adrenal gland function was impaired as indicated by their dampened response to capture and handling and to injections of adrenocorticotropic hormone compared to controls. Approximately 24 hours after consumption of exogenous cortisol, individuals had much lower plasma cortisol concentrations than controls, but adrenal function was restored. Corticosteroid binding globulin (CBG) concentrations were also significantly reduced in squirrels treated with cortisol. Despite these profound shifts in the functionality of the HPA axis, squirrel body mass, offspring survival, and adult survival were unaffected by experimental increases in cortisol concentrations. Our results highlight that even short-term experimental increases in glucocorticoids can affect adrenal gland functioning and CBG concentrations but without other side-effects.

zoology↗