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Boonstra, R.

Publications and source records attributed to Boonstra, R..

6 recordsLinked to original sources

Hippocampal epigenetic changes associated with population cycle phase in wild voles

Vole and lemming population cycles are an enigma in ecology. Decades of field observations and experimental manipulations have revealed that cycles cannot always be explained by extrinsic factors in the environment, including food availability or predator numbers. Thus, it has been proposed that intrinsic mechanisms, such as adaptive alterations in phenotype during different phases of the cycle, drive population dynamics. However, the mechanisms underlying such phenotypic changes have not been elucidated. We test the hypothesis that epigenetic changes occur over population cycles by comparing whole epigenome DNA methylation changes in brain tissue collected from northern red-backed voles (Clethrionomys rutilus) in a wild, naturally cycling population during the peak, decline, and low years. Overall, the greatest number of differentially methylated CG sites (DMCs) and differentially methylated regions (DMRs) were detected in comparisons between voles from the peak phase and low phase of the cycle. We highlight methylation differences in the promoter region of ATP synthase subunit c (Atp5g3) and an intron of insulin-like growth factor 1 receptor (Igf1R), which may be associated with growth, development, and bioenergetics. There were additional changes in the promoters of members of the cytochrome P450 enzyme family, including Cyp1a1, associated with estrogen metabolism, as well as the promoter of macrophage migration inhibitory factor (Mif), and in an exon of serum/glucocorticoid regulated kinase (Sgk1), which may link changes in stressors to direct brain changes. Our study is the first interrogation into broad epigenetic changes associated with natural population cycle phase in a wild mammal.

ecology↗

Hormones do not make the mole-rat: no steroid hormone signatures of subordinate behavioral phenotypes

In some cooperatively breeding groups, individuals have distinct behavioral characteristics that are often stable and predictable across time. However, in others, like the eusocial naked mole-rat, evidence for behavioral phenotypes is ambiguous. Here, we study whether the naked mole-rat can be divided into discrete phenotypes and if circulating hormone levels underpin these differences. Naked mole-rat colonies consist of a single breeding female and dozens to hundreds of non-reproductive subordinates. The subordinates can potentially be divided into soldiers, who defend the colony; workers, who maintain it; and dispersers, who want to leave it. We established six colonies de novo, tracked them over three years, and assessed the behavior and hormone levels of the subordinates. We found that soldiers tended to be from earlier litters and were higher ranked compared to workers, whereas dispersers were distributed throughout litters and rankings. There was no difference in estradiol, testosterone, or dehydroepiandrosterone (DHEA) levels amongst phenotypes. Progesterone levels were higher in soldiers but this difference appeared to be driven by a few individuals. Principal component analysis demonstrated that soldiers separated into a discrete category relative to workers/dispersers, with the highest ranked loadings being age, weight, and testosterone levels. However, the higher testosterone in soldiers was correlated with large body size instead of strictly behavioral phenotype. Workers and dispersers have more overlap with each other and no hormonal differences. Thus the behavioral variation in subordinate naked mole-rats is likely not driven by circulating steroid hormone levels but rather stems from alternative neural and/or neuroendocrine mechanisms.

animal behavior and cognition↗

Coat color mismatch improves survival of a keystone boreal herbivore: energetic advantages exceed lost camouflage

Climate warming is causing asynchronies between animal phenology and environments. Mismatched traits, like coat color change mismatched with snow, can decrease survival. However, coat change does not serve a singular adaptive benefit of camouflage, and alternate coat change functions may confer advantages that supersede mismatch costs. We found that mismatch reduced rather than increased, autumn mortality risk of snowshoe hares in Yukon by 86.5 %. We suggest that the increased coat insulation and lower metabolic rates of winter acclimatized hares confer energetic advantages to white mismatched hares that reduce their mortality risk. We found that white mismatched hares forage 17-77 minutes less per day than matched brown hares between 0 and -10 {degrees}C, thus lowering their predation risk and increasing survival. We found no effect of mismatch on spring mortality risk, where mismatch occurred at warmer temperatures, suggesting a potential temperature limit where the costs of conspicuousness outweigh energetic benefits.

ecology↗

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↗