The glucocorticoid response to environmental change is not specific to agents of natural selection in wild red squirrels

Petrullo, Lauren; Delaney, David M.; Boutin, Stan; McAdam, Andrew G.; Lane, Jeffrey E.; Boonstra, Rudy; Palme, Rupert; Dantzer, Ben

doi:10.1016/j.yhbeh.2022.105262

Cited by 14 publications

(17 citation statements)

References 67 publications

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“…Lynx exhibit prey-switching from snowshoe hares to red squirrels in the year after hare populations crash (O’Donoghue et al . 1998; Petrullo et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

“…1998). Following prior studies (Petrullo et al . 2022), we binned the hare-lynx cycle into 4 categories based on the location in the cycle: peak hare density (when both hare and lynx density are high), one year post hare peak (when hare density crashes, but lynx density remains high), 2-years post peak (when lynx density crashes), and any other year in the cycle.…”

Section: Methodsmentioning

confidence: 96%

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A future food boom rescues the negative effects of cumulative early-life adversity on adult lifespan in a small mammal

Petrullo,

Delaney,

Boutin

et al. 2023

Preprint

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Challenging or adverse early-life conditions, even when transient, can have long-lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated, even in part, by a high quality later-life environment, then differences in future resource access may explain variation in vulnerability and resilience to early-life adversity. Using 32 years of data on 886 wild North American red squirrels, we test the hypothesis that the negative effects of early-life adversity on lifespan can be mitigated by later-life food abundance. We first define early-life adversities as factors that significantly reduce the likelihood of juvenile survival, and find that they had cumulative negative effects on lifespan. We then show that although experimental supplementation with additional food increases individual lifespan, it did not change the consequences of early-life adversity on longevity. A naturally-occurring future food boom experienced in the second year of life, however, did eliminate the longevity costs of a harsh early-life environment. Together, our results demonstrate that adverse conditions experienced early in life reduce lifespan in red squirrels and thus may influence patterns of natural selection beyond juvenile viability. That these effects can be mitigated by a high-quality future environment suggests a non-deterministic role for early-life conditions on later-life phenotypes, and highlights the importance of evaluating the impact of early-life conditions in the context of an animals entire life course.

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“…Lynx exhibit prey-switching from snowshoe hares to red squirrels in the year after hare populations crash (O’Donoghue et al . 1998; Petrullo et al . 2022).…”

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 96%

A future food boom rescues the negative effects of cumulative early-life adversity on adult lifespan in a small mammal

Petrullo,

Delaney,

Boutin

et al. 2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…[73] elevated squirrel density relatively high number of squirrels living on study area (increased conspecific competition) [42,43,59,74] 1 year following peak in lynx-hare cycle a year characterized by a crash in hare density and expected prey-switching by lynx to red squirrels (increased likelihood of predation) [46] elevated mustelid density relatively high number of nest predators (increased likelihood of predation) [42,64] mean winter temperature relatively cold average winter temperatures (increased thermoregulatory costs) [42,48] large litter x non-mast year litter size mismatched to future food abundance (i.e. a large litter produced in a non-mast year when future food is low) [43,44] elevated squirrel density x later birth date relatively high number of squirrels living on study area and a later birth date (reduced likelihood of territory acquisition) [40,59,72] elevated squirrel density x slow postnatal growth relatively high number of squirrels living on study area and poorer growth (reduced likelihood of territory acquisition)…”

Section: (A) Early-life Adversity Predicts Variation In Juvenile Surv...mentioning

confidence: 99%

A future food boom rescues the negative effects of early-life adversity on adult lifespan in a small mammal

Petrullo,

Delaney,

Boutin

et al. 2024

Proc. R. Soc. B.

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Early-life adversity, even when transient, can have lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated by a high-quality later-life environment, then differences in future resources may explain variable resilience to early-life adversity. Using data from over 1000 wild North American red squirrels, we tested the hypothesis that the costs of early-life adversity for adult lifespan could be offset by later-life food abundance. We identified six adversities that reduced juvenile survival in the first year of life, though only one—birth date—had continued independent effects on adult lifespan. We then built a weighted early-life adversity (wELA) index integrating the sum of adversities and their effect sizes. Greater weighted early-life adversity predicted shorter adult lifespans in males and females, but a naturally occurring food boom in the second year of life ameliorated this effect. Experimental food supplementation did not replicate this pattern, despite increasing lifespan, indicating that the buffering effect of a future food boom may hinge on more than an increase in available calories. Our results suggest a non-deterministic role of early-life conditions for later-life phenotype, highlighting the importance of evaluating the consequences of early-life adversity in the context of an animal's entire life course.

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“…This premise contrasts with the existing evidence of the adaptive role of GC increases (including acute responses) under certain environmental contexts, as they allow the organisms to adjust their physiology to prevailing demands ( [8,11]; see below). Indeed, studies testing for correlations between plasma GC concentrations (both baseline and stress-induced) and fitness components have yielded contrasting results [4,7,[12][13][14]. In this context, recent works have claimed that a negative association between GCs and physiological state is an overly simplistic interpretation of the complexity of GC function, claiming the need to study them from a wider, more integrative perspective [15][16][17][18][19].…”

Section: Introductionmentioning

confidence: 99%

Modelling the role of glucocorticoid receptor as mediator of endocrine responses to environmental challenge

Jimeno,

Rubalcaba

2024

Phil. Trans. R. Soc. B

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Glucocorticoid hormones (GCs) modulate acute ‘stress’ responses in vertebrates, exerting their actions across many physiological systems to help the organism face and overcome challenges. These actions take place via binding to the glucocorticoid receptor (GR), which determines not only the magnitude of the GC-mediated physiological response but also the negative feedback that downregulates GCs to restore homeostasis. Although GR function is assumed to determine GC regulation capacity, the associations between GR abundance and individuals' coping abilities remain cryptic. We developed a dynamic model fitted to empirical data to predict the effects of GR abundance on both plasma GC response patterns and the magnitude of GC-mediated physiological response. Individuals with higher GRs showed lower GC exposure, stronger physiological responses and greater capacity to adjust this response according to stressor intensity, which may be translated into more resilient and flexible GC phenotypes. Our results also show that among-individual variability in GR abundance challenges the detectability of the association between plasma GC measurements and physiological responses. Our approach provides mechanistic insights into the role of GRs in plasma GC measurements and function, which point at GR abundance fundamentally driving complex features of the GC regulation system in the face of environmental change. This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.

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The glucocorticoid response to environmental change is not specific to agents of natural selection in wild red squirrels

Cited by 14 publications

References 67 publications

A future food boom rescues the negative effects of cumulative early-life adversity on adult lifespan in a small mammal

A future food boom rescues the negative effects of cumulative early-life adversity on adult lifespan in a small mammal

A future food boom rescues the negative effects of early-life adversity on adult lifespan in a small mammal

Modelling the role of glucocorticoid receptor as mediator of endocrine responses to environmental challenge

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