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Mismatches between an organism’s phenotype and its environment can result in short-term fitness costs. Here, we show that some phenotype – environment mismatch errors can be explained by asymmetrical costs of different types of errors in wild red squirrels. Mothers that mistakenly increased reproductive effort when signals of an upcoming food pulse were absent were more likely to correctly increase effort when a food pulse did occur. However, mothers that failed to increase effort when cues of an upcoming food pulse were present suffered lifetime fitness costs that could only be offset through food supplementation. In fluctuating environments, such phenotype – environment mismatches may therefore reflect a bias to overestimate environmental cues and avoid making the costliest error, ultimately enhancing lifetime fitness.

Territories are typically defined as spatially exclusive areas that are defended against conspecifics. Given the spatial nature of territoriality, it is inherently density dependent, but the economics of territoriality also depend on the distribution and abundance of defended resources. Our objectives were to assess the effects of changing population density and food availability on individually based territorial phenotypes. We developed a novel analytical framework that bridges spatially explicit territories with social network analysis to model density-dependent territorial phenotypes. Using the outputs from our data pipeline, we modelled plasticity in territory size and territory intrusion rates in a long-term study population of North American red squirrels Tamiasciurus hudsonicus. Red squirrels defend year-round territories around a central hoard (midden) of white spruce Picea glauca cones. Importantly, white spruce is a masting species that produces large cone crops every 4-7 years (i.e. mast years) in our study area interspersed with non-mast years when few cones are produced. In the spring following mast years, populations are approximately double in size, but are lower in the spring of non-mast years. We predicted that territory size and intrusion rates would decrease as resource abundance, and consequently population density, increased. By contrast, as resource abundance decreased via depletion, and therefore density decreased, territories should increase in size and intrusions should also increase. As we expected, individual territory size and territorial intrusions were negatively density dependent, such that increased density after mast years resulted in smaller territories and fewer intrusions. When considering between-individual variation in plasticity across a density gradient, individuals responded differently to changes in population density within their lifetime. Our results show that territory size and intrusion rates display negative density dependence. When food becomes available in the autumn of a mast year and density in spring of the following year increases, territories shrink in size to effectively a small area around the midden. While our findings for red squirrels are unique compared to other systems, they serve as a reminder that the direction and strength of fundamental ecological relationships can depend on the nature of the system.

For regions that were covered by ice during the Pleistocene glaciations, species must have emigrated from unglaciated regions. However, it can be difficult to discern when and from what ancestral source populations such expansions took place, especially since warming climates introduce the possibility of very recent expansions. For example, in the Great Lakes region, pronounced climatic change includes past glaciations as well as recent, rapid warming. Here we evaluate different expansion hypotheses with a genomic study of the white-footed mouse (Peromyscus leucopus noveboracensis), which is one of the most common mammals throughout the Great Lakes region. Ecological surveys coupled with historical museum records suggest a recent range expansion of P. leucopus associated with the warming climate over the last decades. These detailed records have yet to be complemented by genomic data that provide the requisite resolution for detecting recent expansion, although some mitochondrial DNA (mtDNA) sequences have suggested possible hypotheses about the geography of expansion. With more than 7,000 loci generated using RADseq, we evaluate support for multiple hypotheses of a geographic expansion in the Upper Peninsula of Michigan (UP). Analysis of a single random single-nucleotide polymorphism per locus revealed a fine-scale population structure separating the Lower Peninsula (LP) population from all other populations in the UP. We also detected a genetic structure that reflects an evolutionary history of postglacial colonization from two different origins into the UP, one coming from the LP and one coming from the west. Instead of supporting a climate-driven range expansion, as suggested by field surveys, our results support more ancient postglacial colonization of the UP from two different ancestral sources. With these results, we offer new insights about P. leucopus geographic expansion history, as well as a more general phylogeographic framework for testing range shifts in the Great Lakes region.

Estimates of body condition are regularly made in wildlife studies, particularly those focused on individual and/or population performance; however, many studies assume that it is always beneficial to be heavier or have a higher body condition index (BCI), without accounting for the physiological significance of variation in the composition of tissues that differ in their function such as fat and lean mass.We hypothesized that the relationship between BCI and masses of physiologically important tissues (fat and lean) would be conditional on the annual patterns of energy acquisition and expenditure of individuals under study, and tested relationships in three species with contrasting ecologies in their respective natural ranges: an obligate hibernator (Columbian ground squirrel,Urocitellus columbianus), a facultative hibernator (black-tailed prairie dog,Cynomys ludovicianus), and a food-caching non-hibernator (North American red squirrel,Tamiasciurus hudsonicus).We measured fat and lean mass in adult males and females of these three species using quantitative magnetic resonance (QMR). We measured body mass, two measures of skeletal structure (zygomatic width and right hind foot length) to develop sex- and species-specific BCIs, and tested the utility of BCI to predict body composition in each species.Body condition indices were more consistently and more strongly correlated with lean mass than fat mass. The indices were most positively correlated with fat when fat was expected to be very high (pre-hibernation prairie dogs). However, in all cases, fat and lean mass were better predicted by overall body mass rather than BCI.These results support our hypothesis that the utility of BCI in estimating fat is conditional on the natural history and annual energetic patterns of the species with regards to expected energy balances at the time of sampling, but measuring body mass alone is likely capturing sufficient variation in fat and lean masses in most cases.

Animals cope with environmental perturbations through the stress response, a set of behavioural and physiological responses aimed to maintain and/or return to homeostasis and enhance fitness. Vertebrate neuroendocrine axis activation in response to environmental stressors can result in the secretion of glucocorticoids (GCs), whose acute increases may be adaptive, while chronic elevation may be detrimental. Invasive grey squirrels ( Sciurus carolinensis ) act as a stressor eliciting elevation of GCs in native red squirrels ( Sciurus vulgaris ). Here we used 6-year data of variation in faecal glucocorticoid metabolite (FGM) concentrations following invasion by grey squirrels in three red squirrel populations, to identify if red squirrels showed physiological habituation to this stressor. The decrease in FGMs over time was more pronounced shortly after invasion and at high densities of grey squirrels while it decreased less strongly and was no longer influenced by the invader density as time since invasion elapsed. At the individual level, FGMs also decreased more markedly as each red squirrel experienced prolonged contact with the invader. Our study provides compelling new data suggesting that native species in the wild can habituate to prolonged contact with invasive species, showing that they may avoid the potentially harmful effects of chronic elevations in GCs.

Animal species vary in whether they provide parental care or the type of care provided, and this variation in parental care among species has been a common focus of comparative studies. However, the proximate causes and ultimate consequences of within-species variation in parental care have been less studied. Most studies about the impacts of within-species variation in parental care on parental fitness have been in primates, whereas studies in laboratory rodents have been invaluable for understanding what causes inter-individual variation in parental care and its influence on offspring characteristics. We integrated both of these perspectives in our long-term study of North American red squirrels (Tamiasciurus hudsonicus) in the Yukon, Canada, where we have focused on understanding the impacts of mothers on offspring. This includes documenting the impacts that mothers or the maternal environment itself has on their offspring, identifying how changes in maternal physiology impact offspring characteristics, the presence of individual variation in maternal attentiveness toward offspring before weaning and its fitness consequences, and postweaning maternal care and its fitness consequences. We provide an overview of these contributions to understanding the impacts mothers have on their offspring in red squirrels using an integrative framework and contrast them with studies in the laboratory.

A wide range of species have been found to differentiate kin from nonkin. However, the ability to recognize kin, or the costs and benefits of discriminating kin from nonkin may depend on particular extrinsic environmental or intrinsic physiological conditions, resulting in context-dependent kin discrimination. North American red squirrels, Tamiasciurus hudsonicus, have previously been shown to be capable of discriminating the territorial calls of kin and nonkin. More recently, post hoc analysis of existing data suggested that kin discrimination might depend on the state of the caller (i.e. acute stress). Here we tested this hypothesis with independently collected data from a repeated-measures playback experiment and found no evidence in support of acute stress mediating kin discrimination. While squirrels were shown to register and respond to playbacks, exposure to a trapping/handling stressor in the caller had no effect on the receiver's response to the calls of kin and nonkin. Furthermore, we found no overall discrimination between the calls of kin and nonkin. These independently collected data instead suggest that the previous post hoc finding consistent with context-dependent kin discrimination was likely a spurious relationship associated with the data from which the post hoc hypothesis was generated rather than representing a real biological relationship. Our findings from this study emphasize the importance of testing post hoc hypotheses with independent experiments.

Understanding the causes and consequences of repeatable among-individual differences in behavior (i.e., animal personality) is a major area of research in behavioral and evolutionary ecology. Recently, attention has turned to understanding the processes behind changes in repeatability through ontogeny because of their implications for populations. We evaluated the relative importance of selective disappearance (i.e., differential mortality), an among-individual mechanism, in generating age-related changes in the repeatability of aggression and activity in juvenile North American red squirrels (Tamiasciurus hudsonicus). We observed age-related decreases in the repeatability of aggression across ages, arising from lower among-individual variance. Although we found evidence for directional selection on aggressiveness, it was insufficient to erode among-individual variance. Thus, ontogenetic decreases in the repeatability of aggression do not appear to be due to selective disappearance. In contrast, the repeatability of activity was higher across ages due to higher among-individual variance in activity, but there was no support for selective disappearance based on activity. Taken together, our results suggest that age-related changes in trait repeatability in red squirrels are not the result of selective disappearance and instead may be the result of within-individual developmental processes, such as individual differences in developmental trajectories.

This is a manuscript version of an article published as: Haines, J.A., Nason, S.E., Skurdal, A.M.M., Bourchier, T., Boutin, S., Taylor, R.W., McAdam, A.G., Lane, J.E., Kelley, A.D., Humphries, M.M., Gorrell, J.C., Dantzer, B., Coltman, D.W., & Hämäläinen, A. (2020). Sex- and context-specific associations between personality and a measure of fitness but no link with life history traits. Animal Behaviour, 167, 23-29. https://doi.org/10.1016/j.anbehav.2020.06.013 The pace-of-life syndrome hypothesis posits that personality traits (i.e. consistent individual differences in behaviour) are linked to life history and fitness. Specifically, fast-paced individuals are predicted to be proactive (i.e. active and aggressive) with an earlier age at first reproduction, a shorter life span and higher fecundity than slow-paced individuals. Environmental conditions and sex differences may be important in maintaining behavioural and life history variation in populations and may influence the covariance of personality with life history or lifetime fitness. However, these effects are rarely tested together. We investigated whether the occurrence of a resource pulse (called a mast year) during adulthood altered the associations between personality and life history traits or lifetime offspring production in adult North American red squirrels, Tamiasciurus hudsonicus. Despite accounting for environmental context during adulthood, we found no evidence of an overall pace-of-life syndrome in this population as personality was not associated with age at first reproduction or longevity in either sex. Males and females had similar activity levels, but females were more aggressive, potentially due to the fitness benefits of protecting their offspring from predation. In all females, regardless of mast experience, there was no association between activity and lifetime pup production, but there was a positive association between aggression and lifetime pup production. In males that experienced a mast, there was a positive association between lifetime pup production and both activity and aggression. In males that did not experience a mast, there was no association between activity and lifetime pup production, but there was a negative association between aggression and lifetime pup production. Lifetime recruit production (number of adult offspring recruited into the breeding population) in either sex was not influenced by activity or aggression regardless of mast experience. Overall, our results suggest that the infrequent occurrence of mast years may contribute to maintaining variation in personality traits in red squirrels. Pre-print version This is a manuscript version of an article published as: Haines, J.A., Nason, S.E., Skurdal, A.M.M., Bourchier, T., Boutin, S., Taylor, R.W., McAdam, A.G., Lane, J.E., Kelley, A.D., Humphries, M.M., Gorrell, J.C., Dantzer, B., Coltman, D.W., & Hämäläinen, A. (2020). Sex- and context-specific associations between personality and a measure of fitness but no link with life history traits. Animal Behaviour, 167, 23-29. https://doi.org/10.1016/j.anbehav.2020.06.013 https://viurrspace.ca/bitstream/handle/10613/23323/GorrellAB.pdf?sequence=3

Animals switch between inactive and active states, simultaneously impacting their energy intake, energy expenditure and predation risk, and collectively defining how they engage with environmental variation and trophic interactions. We assess daily activity responses to long-term variation in temperature, resources and mating opportunities to examine whether individuals choose to be active or inactive according to an optimisation of the relative energetic and reproductive gains each state offers. We show that this simplified behavioural decision approach predicts most activity variation (R2 = 0.83) expressed by free-ranging red squirrels over 4 years, as quantified through accelerometer recordings (489 deployments; 5066 squirrel-days). Recognising activity as a determinant of energetic status, the predictability of activity variation aggregated at a daily scale, and the clear signal that behaviour is environmentally forced through optimisation of gain, provides an integrated approach to examine behavioural variation as an intermediary between environmental variation and energetic, life-history and ecological outcomes.

Tables reporting full models output and comparison, as well as figure showing red and grey squirrel density indexes in the three study sites.

Significant gaps remain in understanding the response of plant reproduction to environmental change. This is partly because measuring reproduction in long-lived plants requires direct observation over many years and such datasets have rarely been made publicly available. Here we introduce MASTREE+, a data set that collates reproductive time-series data from across the globe and makes these data freely available to the community. MASTREE+ includes 73,828 georeferenced observations of annual reproduction (e.g. seed and fruit counts) in perennial plant populations worldwide. These observations consist of 5971 population-level time-series from 974 species in 66 countries. The mean and median time-series length is 12.4 and 10 years respectively, and the data set includes 1122 series that extend over at least two decades (≥20 years of observations). For a subset of well-studied species, MASTREE+ includes extensive replication of time-series across geographical and climatic gradients. Here we describe the open-access data set, available as a.csv file, and we introduce an associated web-based app for data exploration. MASTREE+ will provide the basis for improved understanding of the response of long-lived plant reproduction to environmental change. Additionally, MASTREE+ will enable investigation of the ecology and evolution of reproductive strategies in perennial plants, and the role of plant reproduction as a driver of ecosystem dynamics. EEA Santa Cruz Fil: Hacket-Pain, Andrew. University of Liverpool. School of Environmental Sciences. Department of Geography and Planning; Reino Unido Fil: Foest, Jessie J. University of Liverpool. School of Environmental Sciences. Department of Geography and Planning; Reino Unido Fil: Pearse, Ian S. U.S. Fort Collins Science Center. Geological Survey; Estados Unidos Fil: LaMontagne, Jalene M. DePaul University. Department of Biological Sciences; Estados Unidos Fil: Koenig, Walter D. University of California Berkeley. Hastings Reservation; Estados Unidos Fil: Vacchiano, Giorgio. University of Milan. Milan Department of Agricultural and Environmental Sciences; Italia. Fil: Bogdziewicz, Michał. Adam Mickiewicz University. Faculty of Biology. Institute of Environmental Biology; Polonia Fil: Bogdziewicz, Michał. University Grenoble Alpes. INRAE, LESSEM; Francia Fil: Caignard, Thomas. Université Bordeaux. INRAE, BIOGECO; Francia Fil: Celebias, Paulina. Adam Mickiewicz University. Faculty of Biology. Institute of Environmental Biology; Polonia Fil: Peri, Pablo Luis. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Santa Cruz; Argentina. Fil: Peri, Pablo Luis. Universidad Nacional de la Patagonia Austral; Argentina. Fil: Peri, Pablo Luis. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Fil: Ascoli, Davide. University of Torino. Department of Agricultural. Forest and Food Sciences (DISAFA); Italia Fil: Gallo, Leonardo Ariel. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Bariloche; Argentina Fil: Gallo, Leonardo Ariel. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones Forestales y Agropecuarias Bariloche; Argentina Fil: Marchelli, Paula. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Bariloche; Argentina Fil: Marchelli, Paula. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Instituto de Investigaciones Forestales y Agropecuarias Bariloche; Argentina

While cooperative interactions among kin are a key building block in the societies of group-living species, their importance for species with more variable social environments is unclear. North American red squirrels ( Tamiasciurus hudsonicus ) defend individual territories in dynamic neighbourhoods and are known to benefit from living among familiar conspecifics, but not relatives. However, kin-directed behaviours may be restricted to specific genealogical relationships or strongly mediated by geographical distance, masking their influence at broader scales. Using distance between territories as a proxy for the ability of individuals to interact, we estimated the influence of primary kin (parents, offspring, siblings) on the annual survival and reproductive success of red squirrels. This approach revealed associations between fitness and access to kin, but only for certain genealogical relationships and fitness components. For example, females had enhanced annual survival when living closer to their daughters, though the reverse was not true. Most surprising was the finding that males had higher annual reproductive success when living closer to their father, suggesting possible recognition and cooperation among fathers and sons. Together, these findings point to unexpected nuance in the fitness consequences of kinship dynamics for a species that is territorial and largely solitary.

Sleep is appreciated as a behavior critical to homeostasis, performance, and fitness. Yet, most of what we know about sleep comes from humans or controlled laboratory experiments. Assessing sleep in wild animals is challenging, as it is often hidden from view, and electrophysiological recordings that define sleep states are difficult to obtain. Accelerometers have offered great insight regarding gross movement, although ambiguous quiescent states like sleep have been largely ignored, limiting our understanding of this ubiquitous behavior.We developed a broadly applicable sleep detection method called a homeogram that can be applied to accelerometer data collected from wild animals. We applied our methodology to detect sleep in free-ranging North American red squirrels (Tamiasciurus hudsonicus) in a region that experiences drastic seasonal shifts in light, temperature, and behavioral demands.Our method characterized sleep in a manner consistent with limited existing studies and expanded those observations to provide evidence that red squirrels apply unique sleep strategies to cope with changing environments.Applying our analytical strategy to accelerometer data from other species may open new possibilities to investigate sleep patterns for researchers studying wild animals.

The episodic production of large seed crops by some perennial plants, is referred to as masting and is known to increase seed escape by alternately starving and swamping seed predators. These pulses of resources, however, might also act as an agent of selection on the life histories of seed predators, which could indirectly enhance seed escape by inducing an evolutionary load on seed predator populations. Lag loads in seed predators could result from mast-induced shifts in optimum phenotypes that exceed the capacity of seed predators to adaptively track optimum phenotypes through phenotypic plasticity. Alternatively, masting could generate mismatches in selection across generations, where adaptation to the parental environment leads to maladaptation in the offspring environment. Here we measured natural selection on female North American red squirrels (Tamiasciurus hudsonicus) across 28 years and five white spruce (Picea glauca) masting events. Red squirrel litter sizes were similar to optimum litter sizes during non-mast years, but were well below optimum litter sizes during resource-rich mast years. Mast events, therefore caused selection for larger litters (B = 0.25) and a lag load (L = 0.25) on red squirrels during mast years. Furthermore, we found that the annual fitness of spruce trees was negatively related to the local density of squirrels during mast years, indicating that the observed lag load on squirrels enhanced the number of spruce cones escaping squirrel predation. Although, the frequency of mast events and the demography of red squirrels were such that offspring and parents often experienced opposite environments with respect to the mast, we found no effect of environmental mismatches across generations on either offspring survival or population growth. Instead, squirrels plastically increased litter sizes in anticipation of mast events, which partially, although not completely, reduced the lag load resulting from this change in food availability. Variable selection on litter size caused by white spruce mast events, therefore, induced a lag load on the population of red squirrels that was not affected by whether individual squirrels were born during mast (matching) or non-mast (mismatching) conditions.

For territorial species, the ability to be behaviourally plastic in response to changes in their social environment may be beneficial by allowing individuals to mitigate conflict with conspecifics and reduce the costs of territoriality. Here we investigated whether North American red squirrels, Tamiasciurus hudsonicus, are able to minimize costs of territory defence by adjusting behaviour in response to the familiarity of neighbouring conspecifics. Since red squirrels living in familiar neighbourhoods face reduced intrusion risk, we predicted that increasing familiarity among territorial neighbours would allow squirrels to spend less time on territorial defence and more time in the nest. Longitudinal behavioural data (1995–2004) collected from the same squirrels across several different social environments indicated that red squirrels reduced rates of territorial vocalizations and increased nest use in response to increasing familiarity with neighbours. In contrast, cross-sectional data (2015–2016), which provided observations from each individual in a single social environment, did not provide evidence of this plasticity. Post hoc analyses revealed that evidence of social plasticity in this system is primarily due to within-individual changes in behaviour, which we were unable to estimate in the cross-sectional data. Our results demonstrate that red squirrels respond to changes in their social environment by adjusting their behaviour in a manner that reduces the costs of territoriality. However, our results also suggest that estimating plasticity by comparing behaviour among individuals (i.e. cross-sectional analyses) may not always be reliable. Our ability to detect these effects may therefore depend on having data with multiple observations from the same individuals across different social environments.

Acoustic signaling is an important means by which animals communicate both stable and labile characteristics. Although it is widely appreciated that vocalizations can convey information on labile state, such as fear and aggression, fewer studies have experimentally examined the acoustic expression of stress state. The transmission of such public information about physiological state could have broad implications, potentially influencing the behavior and life-history traits of neighbors. North American red squirrels (Tamiasciurus hudsonicus) produce vocalizations known as rattles that advertise territorial ownership. We examined the influence of changes in physiological stress state on rattle acoustic structure through the application of a stressor (trapping and handling the squirrels) and by provisioning squirrels with exogenous glucocorticoids (GCs). We characterized the acoustic structure of rattles emitted by these squirrels by measuring rattle duration, mean frequency, and entropy. We found evidence that rattles do indeed exhibit a “stress signature.” When squirrels were trapped and handled, they produced rattles that were longer in duration with a higher frequency and increased entropy. However, squirrels that were administered exogenous GCs had similar rattle duration, frequency, and entropy as squirrels that were fed control treatments and unfed squirrels. Our results indicate that short-term stress does affect the acoustic structure of vocalizations, but elevated circulating GC levels do not mediate such changes.

Organisms can affect one another's phenotypes when they socially interact. Indirect genetic effects occur when an individual's phenotype is affected by genes expressed in another individual. These heritable effects can enhance or reduce adaptive potential, thereby accelerating or reversing evolutionary change. Quantifying these social effects is therefore crucial for our understanding of evolution, yet estimates of indirect genetic effects in wild animals are limited to dyadic interactions. We estimated indirect phenotypic and genetic effects, and their covariance with direct effects, for the date of spring breeding in North American red squirrels (Tamiasciurus hudsonicus) living in an array of territories of varying spatial proximity. Additionally, we estimated indirect effects and the strength of selection at low and high population densities. Social effects of neighbours on the date of spring breeding were different from zero at high population densities but not at low population densities. Indirect phenotypic effects accounted for a larger amount of variation in the date of breeding than differences attributable to the among-individual variance, suggesting social interactions are important for determining breeding dates. The genetic component to these indirect effects was however not statistically significant. We therefore showcase a powerful and flexible method that will allow researchers working in organisms with a range of social systems to estimate indirect phenotypic and genetic effects, and demonstrate the degree to which social interactions can influence phenotypes, even in a solitary species.

Evolutionary endocrinology aims to understand how natural selection shapes endocrine systems and the degree to which endocrine systems themselves can induce phenotypic responses to environmental changes. Such responses may be specialized in that they reflect past selection for responsiveness only to those ecological factors that ultimately influence natural selection. Alternatively, endocrine responses may be broad and generalized, allowing organisms to cope with a variety of environmental changes simultaneously. Here, we empirically tested whether the endocrine response of female North American red squirrels (Tamiasciurus hudsonicus) was specialized or generalized. We first quantified the direction and magnitude of natural selection acting on three female life history traits (parturition date, litter size, offspring postnatal growth rate) during 32 years of fluctuations in four potential ecological agents of selection (food availability, conspecific density, predator abundance, and temperature). Only three of the four variables (food, density, and predators) affected patterns of natural selection on female life history traits. We then quantified fecal glucocorticoid metabolites (FGMs) across 7 years and found that all four environmental variables, regardless of their effects on patterns of selection, were associated with glucocorticoid production. Our results provide support for a generalized, rather than specific, glucocorticoid response to environmental change that can integrate across multiple co-occurring environmental stressors.

The effect of the social environment on individual state or condition has largely focused on glucocorticoid levels (GCs). As metabolic hormones whose production can be influenced by nutritional, physical, or psychosocial stressors, GCs are a valuable (though singular) measure that may reflect the degree of "stress" experienced by an individual. Most work to date has focused on how social rank influences GCs in group-living species or how predation risk influences GCs in prey. This work has been revealing, but a more comprehensive assessment of the social environment is needed to fully understand how different features of the social environment influence GCs in both group living and non-group living species and across life history stages. Just as there can be intense within-group competition among adult conspecifics, it bears appreciating there can also be competition among siblings from the same brood, among adult conspecifics that do not live in groups, or among heterospecifics. In these situations, dominance hierarchies typically emerge, albeit, do dominants or subordinate individuals or species have higher GCs? We examine the degree of support for hypotheses derived from group-living species about whether differential GCs between dominants and subordinates reflect the "stress of subordination" or "costs of dominance" in these other social contexts. By doing so, we aim to test the generality of these two hypotheses and propose new research directions to broaden the lens that focuses on social hierarchies and GCs.

Animals in urban areas that experience frequent exposure to humans often behave differently than those in less urban areas, such as exhibiting less vigilance or anti-predator behavior. These behavioral shifts may be an adaptive response to urbanization, but it may be costly if animals in urban areas also exhibit reduced anti-predator behavior in the presence of natural predators. In trials with only a human observer as the stimulus, urban squirrels exhibited reduced vigilance and anti-predator behavior compared to those in less urban areas. Next, we exposed squirrels in multiple urban and less urban sites to acoustic playbacks of a control stimulus (non-predatory bird calls), a natural predator (hawk), and dogs and recorded their vigilance and three different anti-predator behaviors when a human approached them while either broadcasting one of these three playbacks or no playbacks at all. Squirrels at urban sites also did not differ in their behavioral responses to the playbacks from possible predators (hawks or dogs) when they were compared to those at less urban sites exposed to these playbacks. Urban squirrels also exhibited increased vigilance and anti-predator behavior when exposed to a human paired with hawk playbacks compared to the control playbacks. Together, our results indicate that urban squirrels did perceive and assess risk to the natural predator appropriately despite exhibiting increased tolerance to humans. These results provide little support for the hypothesis that increased tolerance to humans causes animals to lose their fear of natural predators.

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.

As a response to environmental cues, maternal glucocorticoids (GCs) may trigger adaptive developmental plasticity in the physiology and behavior of offspring. In North American red squirrels (Tamiasciurus hudsonicus), mothers exhibit increased GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under these conditions. We tested the hypothesis that elevated maternal GCs cause shifts in offspring behavior that may prepare them for high-density conditions. We experimentally elevated maternal GCs during gestation or early lactation. We measured two behavioral traits (activity and aggression) in weaned offspring using standardized behavioral assays. Because maternal GCs may influence offspring hypothalamic–pituitary–adrenal (HPA) axis dynamics, which may in turn affect behavior, we also measured the impact of our treatments on offspring HPA axis dynamics (adrenal reactivity and negative feedback), and the association between offspring HPA axis dynamics and behavior. Increased maternal GCs during lactation, but not gestation, slightly elevated activity levels in offspring. Offspring aggression and adrenal reactivity did not differ between treatment groups. Male, but not female, offspring from mothers treated with GCs during pregnancy exhibited stronger negative feedback compared with those from control mothers, but there were no differences in negative feedback between lactation treatment groups. Offspring with higher adrenal reactivity from mothers treated during pregnancy (both controls and GC-treated) exhibited lower aggression and activity. These results suggest that maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce substantial changes in behavioral and physiological stress responses in offspring in natural populations.

Parental investment theory predicts that observed levels of parental care afforded to offspring are set by the benefits (to offspring quality and survival) relative to the costs (to parental survival or future reproduction). Although difficult to document in mammals, there is often substantial individual variation in the amount of parental care within species. We measured the impact of individual variation in maternal care (“attentiveness” towards offspring or maternal motivation) on offspring growth and survival in a wild population of North American red squirrels (Tamiasciurus hudsonicus). We used latency to return to pups following a nest intrusion as a measure of maternal attentiveness to pups. We found this behavior to be repeatable within individuals suggesting this behavior is a personality trait or a “maternal style.” In this population, postnatal growth rate is important for pup overwinter survival. Pups from large litters grew faster if they had a highly attentive mother, indicating that maternal care can mitigate the trade-off between litter size and offspring growth and potentially improve survival of pups. Additionally, more attentive mothers had slightly higher lifetime reproductive success than less attentive mothers. These results highlight important fitness effects of having a highly attentive mother and show that maternal care can alter a fundamental life history trade-off between offspring quantity and quality. It pays to be attentive to your pups as a squirrel mom. In a long-term study of a wild population of North American red squirrels, we tested whether maternal behavior was predictive of growth rate and survival of offspring. To do this, we observed maternal attentiveness towards offspring by recording the time until the mother returned to her pups following a nest intrusion by researchers. We found repeatable individual variation in maternal attentiveness suggesting consistent “maternal styles” among individuals. Mothers who returned faster to pups following a nest intrusion produced faster growing pups and were able to produce larger fast-growing litters. Over their entire lifetime, attentive mothers also had more offspring survive to adulthood.

Interactions between organisms are ubiquitous and have important consequences for phenotypes and fitness. Individuals can even influence those they never meet, if they have extended phenotypes that alter the environments others experience. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is usually subsequently acquired by non-relatives. Hoarding by previous owners can, therefore, influence subsequent owners. We found that red squirrels breed earlier and had higher lifetime fitness if the previous hoard owner was a male. This was driven by hoarding behaviour, as males and mid-aged squirrels had the largest hoards, and these effects persisted across owners, such that if the previous owner was male or died in mid-age, subsequent occupants had larger hoards. Individuals can, therefore, influence each other's resource-dependent traits and fitness without ever meeting, such that the past can influence contemporary population dynamics through extended phenotypes.

Free-living animals cope with environmental stressors through physiological and behavioural responses. According to the unidimensional model, these responses are integrated within a coping style: proactive individuals (bold, active-explorative and social) have a lower hypothalamic-pituitary-adrenal (HPA) axis reactivity than reactive ones (shy, less active-explorative, less social). These associations may change when individuals are exposed to human-induced rapid environmental change (HIREC), such as the introduction of invasive alien species (IAS). Here, we studied Eurasian red squirrels to investigate the relationship between personality traits and one integrated measure of HPA axis activity, both in areas uncolonized (natural populations) and colonized by an IAS, the Eastern grey squirrel (invaded populations). We expected an association between physiological and behavioural responses, and that activity, exploration and social tendency would covary, forming a behavioural syndrome in natural populations, while competition with the IAS was predicted to disrupt these associations. We used faecal glucocorticoid metabolites (FGMs) as an integrated measure of adrenocortical activity, and measured the levels of four personality traits (exploration, activity, activity-exploration and social tendency) with an open field test and a mirror image stimulation test. We found no correlation between FGMs and personality traits, neither in natural nor invaded populations. However, we found correlations among personality traits in areas without interspecific competition, indicating a behavioural syndrome, which was disrupted in invaded populations. This is one of the few studies showing that an IAS, acting as an environmental stressor, alters a native species' behavioural syndrome, but does not influence its coping style.

The causes and consequences of individual differences in animal behavior and stress physiology are increasingly studied in wild animals, yet the possibility that stress physiology underlies individual variation in social behavior has received less attention. In this review, we bring together these study areas and focus on understanding how the activity of the vertebrate neuroendocrine stress axis (HPA‐axis) may underlie individual differences in social behavior in wild animals. We first describe a continuum of vertebrate social behaviors spanning from initial social tendencies (proactive behavior) to social behavior occurring in reproductive contexts (parental care, sexual pair‐bonding) and lastly to social behavior occurring in nonreproductive contexts (nonsexual bonding, group‐level cooperation). We then perform a qualitative review of existing literature to address the correlative and causal association between measures of HPA‐axis activity (glucocorticoid levels or GCs) and each of these types of social behavior. As expected, elevated HPA‐axis activity can inhibit social behavior associated with initial social tendencies (approaching conspecifics) and reproduction. However, elevated HPA‐axis activity may also enhance more elaborate social behavior outside of reproductive contexts, such as alloparental care behavior. In addition, the effect of GCs on social behavior can depend upon the sociality of the stressor (cause of increase in GCs) and the severity of stress (extent of increase in GCs). Our review shows that the while the associations between stress responses and sociality are diverse, the role of HPA‐axis activity behind social behavior may shift toward more facilitating and less inhibiting in more social species, providing insight into how stress physiology and social systems may co‐evolve.

Territoriality arises when the benefits of resources exceed the costs of defending them. The dear enemy phenomenon, where familiar territorial neighbours refrain from intruding on one another and mutually reduce their defensive efforts, allows for reduction of these costs but requires discrimination between conspecifics. We hypothesized that territorial vocalizations in red squirrels (Tamiasciurus hudsonicus) are used for this discrimination. We performed a speaker replacement experiment where red squirrels () were temporarily removed from their territories and replaced with a speaker broadcasting their own call, an unfamiliar call, or silence. Contrary to our prediction, there were no differences in overall intrusion risk among our three playbacks, but the identity of intruders did vary. Existing variation in familiarity within territorial neighbourhoods should be considered, rather than the binary classification of familiar or stranger, when studying dear enemy effects. We also discuss the variable importance of silence in acoustic territorial populations.

Interactions with conspecifics are an important aspect of an individual's environment. Although it is well known that the presence of conspecifics can have important effects on behaviour, in general it is also now acknowledged that the composition of the social environment can vary, and that this variation may have profound effects on individual behaviour and fitness. Using a wild population of North American red squirrels, Tamiasciurus hudsonicus, we investigated the importance of the composition of the social environment in a territorial species by assessing whether the risk of intrusion faced by territory owners varied with the degree of relatedness and familiarity in their social neighbourhoods. To test this, we conducted temporary removals of territory owners and observed the time until intrusion and the identity of intruding individuals. We found that individuals in neighbourhoods with low average familiarity faced a higher risk of intrusion and that unfamiliar neighbours were more likely to intrude. Surprisingly, we found that related neighbours also posed a higher risk of intrusion. The results from our study suggest that familiarity with neighbours may be an ecologically and evolutionarily relevant measure of the social environment, even in a species considered to be ‘asocial’. Future studies should consider the potential importance of the social environment, which has heretofore been mostly overlooked, as a relevant selective pressure in asocial, territorial species.

Nearly all animals interact with members of their own species at some point during their lives. These behavioral interactions range from courtship, mating, and parental care to the complex cooperative behavior among related or unrelated individuals in group-living species. A number of theoretical models have attempted to explain how cooperation can evolve through natural selection. Although tremendously influential in animal behavior research, these traditional models have largely ignored individual variation in cooperative behavior and its underlying developmental and proximate mechanisms. However, a set of emerging models suggest that the evolution of cooperation can be heavily influenced by the degree of individual variation in cooperative behavior, as well as the complexity of the underlying mechanisms. Yet, while theoreticians argue the importance of studying individual variation in cooperation and the mechanisms underlying it, empiricists have not focused upon these aspects. The main objectives of our symposium at the 2017 meeting of the Society for Integrative and Comparative Biology is to establish new research avenues to study variation in cooperative behavior using both proximate and ultimate explanations and to produce a road map to study the developmental and proximate mechanisms in generating individual variation in cooperative behavior. This symposium brought together empiricists and theoreticians investigating cooperative behavior in diverse taxa and across multiple levels of analysis. Here we briefly describe the rationale for this symposium and why we thought it was needed as well as provide a brief overview of the contributions.

The National Environment Research Council (RG53472 to T.H.C-B.), the European Research Council (294494 to T.H.C-B.), the University of Zurich and the Mammal Research Institute at the University of Pretoria.

Short-term elevation of glucocorticoids (GCs) is one of the major physiological mechanisms by which vertebrates cope with challenging environmental or social factors (stressors). However, when exposure to stressors occurs repeatedly or over a prolonged period of time, animals may experience chronic elevation of GCs, which reduces the immune response efficiency and can lead to higher intensity of parasitic infection. Here, we used invasive gray squirrels Sciurus carolinensis introduced in Northern Italy and their 2 most prevalent gastrointestinal parasites, the nematode Strongyloides robustus and coccidia of the genus Eimeria, as a model to investigate relationships among macroparasite infection and concentrations of fecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs. Our results revealed an association of FGMs with infection by St. robustus, but not with coccidia. Individuals with higher FGMs appear to be responsible for the greatest St. robustus egg shedding within gray squirrel populations, thus possibly acting as superspreaders. However, FGMs were negatively associated with adult St. robustus, suggesting that the abundance of adults of this nematode species does not induce elevation in FGMs, but is only affected by it through immune-mediated effects on its fecundity. Finally, the relationship between St. robustus (both eggs and adult parasites) and FGMs was not linear, suggesting that only high levels of physiological stress influence parasite infection. Our findings highlight that the direction and magnitude of the stress–infection relationship may depend not only on the specific host–parasite system, but also on the different life stages of the same parasite.

Quantifying how whole organisms respond to challenges in the external and internal environment (“stressors”) is difficult. To date, physiological ecologists have mostly used measures of glucocorticoids (GCs) to assess the impact of stressors on animals. This is of course too simplistic as Hans Seyle himself characterized the response of organisms to “noxious stimuli” using multiple physiological responses. Possible solutions include increasing the number of biomarkers to more accurately characterize the “stress state” of animal or just measuring different biomarkers to more accurately characterize the degree of acute or chronic stressors an animal is experiencing. We focus on the latter and discuss how heart rate (HR) and heart rate variability (HRV) may be better predictors of the degree of activation of the sympathetic–adrenal–medullary system and complement or even replace measures of GCs as indicators of animal health, welfare, fitness, or their level of exposure to stressors. The miniaturization of biological sensor technology (“bio-sensors” or “bio-loggers”) presents an opportunity to reassess measures of stress state and develop new approaches. We describe some modern approaches to gathering these HR and HRV data in free-living animals with the aim that heart dynamics will be more integrated with measures of GCs as bio-markers of stress state and predictors of fitness in free-living animals.

Dispersal is nearly universal; yet, which sex tends to disperse more and their success thereafter depends on the fitness consequences of dispersal. We asked if lifetime fitness differed between residents and immigrants (successful between-population dispersers) and their offspring using 29 years of monitoring from North American red squirrels (Tamiasciurus hudsonicus) in Canada. Compared to residents, immigrant females had 23% lower lifetime breeding success (LBS), while immigrant males had 29% higher LBS. Male immigration and female residency were favoured. Offspring born to immigrants had 15-43% lower LBS than offspring born to residents. We conclude that immigration benefitted males, but not females, which appeared to be making the best of a bad lot. Our results are in line with male-biased dispersal being driven by local mate competition and local resource enhancement, while the intergenerational cost to immigration is a new complication in explaining the drivers of sex-biased dispersal.

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.Significance 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.

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.

Comparative studies aid in our understanding of specific conditions favoring the initial evolution of different types of social behaviors, yet there is much unexplained intraspecific variation in the expression of social behavior that comparative studies have not yet addressed. The proximate causes of this individual variation in social behavior within a species have been examined in some species but its fitness consequences have been less frequently investigated. In this study, we quantified the fitness consequences of variation in the sociality of prairie voles (Microtus ochrogaster). We characterized sociality of voles in semi-natural enclosures using an automated behavioral tracking system paired with social network analyses to quantify the degree of spatial and temporal co-occurrence of different voles. We then assessed the relationship between sociality with mating success (number of different conspecifics with which an individual produced offspring) and reproductive success (total number of offspring surviving to first capture). We measured the number of social connections each individual had with all voles and only with opposite-sex voles by calculating unweighted degree through social network analyses. Both female and male voles varied in the number of social connections they had with all conspecifics and with opposite-sex conspecifics. Voles with an intermediate number of social connections with voles of both sexes had higher mating success overall. In our analyses that considered all social connections with voles of both sexes, voles with an intermediate number of social connections produced more offspring. Males with a very high or low number of social connections also had the lowest average body mass. Overall, our results suggest some limit on the fitness benefits of sociality. Although there was substantial individual-variation in our measure of vole social behavior, intermediate levels of social connections may be most favorable.