The endocrine mechanisms causing variation and plasticity in life history traits (e.g., development time, mass at birth/hatching, rate of postnatal growth, age or size at sexual maturity, litter or clutch size, annual survival, and lifespan) or fitness (annual or lifetime reproductive success) have recently garnered considerable interest. We review three issues facing studies that quantify relationships between endocrine traits and life histories or measures of fitness and describe possible solutions using insights from evolutionary ecology. We focus in particular on the steroid hormones glucocorticoids that are involved in the vertebrate neuroendocrine stress response. First, context-dependent associations between endocrine traits and life histories or fitness are widespread, and therefore, it is important to quantify how intrinsic or extrinsic factors modify these relationships. Second, studies in evolutionary endocrinology may aspire to quantify patterns of natural selection on endocrine traits, but this may not tell us how they influence fitness. Studies that also identify the actual targets of selection that the endocrine traits are influencing will be very useful. Third, environmental or intrinsic factors can cause co-variance between endocrine traits and life histories or fitness. This is problematic for interpreting the potential evolutionary consequences of selection on endocrine traits, but it can also produce divergent answers for relationships between endocrine traits and life histories or fitness depending upon whether the data are analyzed in an among- or within-year framework. Future long-term studies following uniquely marked individuals over their lifetime (longitudinal individual-based approach) in combination with experimental manipulations of the endocrine traits or environmental factors influencing both endocrine traits and life histories or fitness may help to produce new insights in evolutionary endocrinology despite these issues. This is an ambitious endeavor, and we briefly review some of the key issues facing such long-term studies and experimental manipulations of endocrine traits.
Glucocorticoids (GCs) are involved in the regulation of an animal’s energetic state. Under stressful situations, they are part of the neuroendocrine response to cope with environmental challenges. Animals react to aversive stimuli also through behavioral responses, defined as coping styles. Both in captive and wild populations, individuals differ in their behavior along a proactive–reactive continuum. Proactive animals exhibit a bold, active-explorative and social personality, whereas reactive ones are shy, less active-explorative and less social. Here, we test the hypothesis that personality traits and physiological responses to stressors covary, with more proactive individuals having a less pronounced GC stress response. In wild populations of invasive gray squirrels Sciurus carolinensis, we measured fecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs, and 3 personality traits (activity, sociability, and exploration) derived from open field test (OFT) and mirror image stimulation (MIS) test. Gray squirrels had higher FGMs in Autumn than in Winter and males with scrotal testes had higher FGMs than nonbreeding males. Personality varied with body mass and population density. Squirrels expressed more activity-exploration at higher than at lower density and heavier squirrels had higher scores for activity-exploration than animals that weighed less. Variation in FGM concentrations was not correlated with the expression of the 3 personality traits. Hence, our results do not support a strong association between the behavioral and physiological stress responses but show that in wild populations, where animals experience varying environmental conditions, the GC endocrine response and the expression of personality are uncorrelated traits among individuals.
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..
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.
19Elevations in glucocorticoid levels (GCs) in breeding females may induce adaptive shifts in 20 offspring life histories. Offspring produced by mothers with elevated GCs may be better 21 prepared to face harsh environments where a faster pace of life is beneficial. We examined how 22 experimentally elevated GCs in pregnant or lactating North American red squirrels 23 (Tamiasciurus hudsonicus) affected offspring growth in body mass, structural (skeletal) size, 24 oxidative stress levels (balance of two antioxidants and one measure of oxidative protein 25 damage) in three different tissues (blood, heart, liver), and liver telomere lengths. We predicted 26 that offspring from mothers treated with GCs would grow faster but would also have higher 27 levels of oxidative stress and shorter telomeres, which may predict reduced longevity. Offspring 28 from mothers treated with GCs during pregnancy grew (in body mass) 17.0% faster than those 29 from controls, whereas offspring from mothers treated with GCs during lactation grew 34.8% 30 slower than those from controls. Treating mothers with GCs during pregnancy or lactation did 31 not alter the oxidative stress levels or telomere lengths of their offspring. Fast-growing offspring 32 from any of the treatment groups did not have higher oxidative stress levels or shorter telomere 33 lengths, indicating that offspring that grew faster early in life (~1 to 25 d of age) did not exhibit 34 oxidative costs after this period of growth, when these measures of oxidative stress and telomere 35 lengths were obtained (~70 d of age). Our results indicate that elevations in maternal GCs may 36 induce plasticity in offspring growth without long-term oxidative costs to the offspring that 37 might result in a shortened lifespan. 38 39
Estimating repeatability of behavioral traits and phenotypic correlations among behavioral 1 traits 2We used the R package 'rptR' version 0.9.21 (Stoffel et al. 2017) to estimate the within-3 individual repeatability of docility in a model lacking any fixed or random effects. Due to the 4 the R package 'MCMCglmm' version 2.25 (Hadfield 2010). The MCMCglmm framework 16 allowed us to test for an among-individual correlation between a trait with repeated measures (in 17 this case, docility) and variables with only one observation per individual (in this case, activity 18 and aggression) by controlling for the lack of within-individual variation of the behavioral trait 19 with only one observation. This model was limited to data from individuals tested for all three 20 behavioral traits (n = 23). 21 22
Adaptive behavioral plasticity can play a beneficial role when a population becomes established in a novel environment if environmental cues allow the expression of appropriate behavior. Further, plasticity itself can evolve over time in a new environment causing changes in the way or degree to which animals respond to environmental cues. Colonization events provide an opportunity to investigate such relationships between behavioral plasticity and adaptation to new environments. Here, we investigated the evolution of behavior and behavioral plasticity during colonization of a new environment, by testing if female mate‐choice behavior diverged in Trinidadian guppies 2–3 years (~6–9 generations) after being introduced to four locations with reduced predation risk. We collected wild‐caught fish from the source and introduced populations, and we reared out second‐generation females in the laboratory with and without predator cues to examine their plastic responses to a bright and dull male. We found introduced females were less responsive to males when reared without predator cues, but both introduced and source females were similarly responsive when reared with predator cues. Thus, the parallel evolution of behavior across multiple populations in the low‐predation environment was only observed in the treatment mimicking the introduction environment. Such results are consistent with theory predicting that the evolution of plasticity is a by‐product of differential selection across environments.
Activity in distinct brain regions reflects behavioral context versus social motivation in a in which behavioral repertoires are shared across social contexts (Trinidadian guppies, Poecilia reticulata).
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