Evolutionary trade-offs in dormancy phenology.

Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the 'life-history' hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.

Down-regulating the stress axis: Living in the present while preparing for the future.

The measurement of glucocorticoid (GC) hormones provides us with a window into the stress physiology of vertebrates and the adaptative responses they use to cope with predictable and unpredictable changes in the environment. Baseline GCs inform us about the metabolic demands they are subject to at that point in their yearly life-history stage, whereas GC changes (often increases) in response to acute challenges inform us on their capacity to cope with more immediate environmental challenges. However, baseline GC levels and the kinetics of GC responses to acute stressors can vary substantially among and within species, depending on individual characteristics (age, sex, condition, life-history stage). In addition, a thorough understanding of the stress status of an animal requires moving beyond the measurement of GCs alone by focusing on downstream measures of metabolic activation, such as oxidative stress. Here, we evaluated the changes in blood cortisol and oxidative stress markers in wild adult Columbian ground squirrels (Urocitellus columbianus), following a 30-min capture-handling stress performed in mid-late June. Measurements were taken when males were post-reproductive and preparing for hibernation and adult females were weaning litters. We found three key results. First, the time-course of GC increase was markedly slower (by an order of magnitude) than what is currently reported in the literature for most species of mammals, birds and reptiles. Second, there were marked differences in the male and female response, linked to differences in life-history stage: females close to weaning had abolished GC responses, whereas post-reproductive males did not. Third, there were mild to moderate increases in oxidative damage and decreases in oxidative defenses in response to our short-term challenge, consistent with the idea that short-term acute metabolic activation may carry physiological costs. However, these changes were not correlated to the changes in GCs, a novel result suggesting a disconnect between the hormonal stress response and oxidative damage.

How much multiple paternity should we expect? A study of birds and contrast with mammals.

Parentage analyses via molecular markers have revealed multiple paternity within the broods of polytocous species, reshaping our understanding of animal behavior, ecology, and evolution. In a meta-analysis of multiple paternity in bird and mammal species, we conducted a literature search and found 138 bird and 64 mammal populations with microsatellite DNA paternity results. Bird populations averaged 19.5% multiple paternity and mammals more than twice that level (46.1%). We used a Bayesian approach to construct a null model for how multiple paternity should behave at random among species, under the assumption that all mated males have equal likelihood of siring success, given mean brood size and mean number of sires. We compared the differences between the null model and the actual probabilities of multiple paternity. While a few bird populations fell close to the null model, most did not, averaging 34.0-percentage points below null model predictions; mammals had an average probability of multiple paternity 13.6-percentage points below the null model. Differences between bird and mammal species were also subjected to comparative phylogenetic analyses that generally confirmed our analyses that did not adjust for estimated historical relationships. Birds exhibited extremely low probabilities of multiple paternity, not only compared to mammals but also relative to other major animal taxa. The generally low probability of multiple paternity in birds might be produced by a variety of factors, including behaviors that reflect sexual selection (extreme mate guarding or unifocal female choice) and sperm competition (e.g., precedence effects favoring fertilization by early or late matings).

Sexes in sync: phenotypic plasticity, sexual selection and phenological synchrony between the sexes in a wild hibernator.

Desynchrony of phenological responses to climate change is a major concern for ecological communities. Potential uncoupling between one of the most fundamental divisions within populations, males and females, has not been well studied. To address this gap, we examined sex-specific plasticity in hibernation phenology in two populations of Columbian ground squirrels (Urocitellus columbianus). We find that both sexes display similar phenological plasticity to spring snowmelt dates in their timing of torpor termination and behavioural emergence from hibernation. As a result of this plasticity, the degree of protandry (i.e. males' emergences from hibernation preceding those of females) did not change significantly over the 27-year study. Earlier male behavioural emergence, relative to females, improved the likelihood of securing a breeding territory and increased annual reproductive success. Sexual selection favouring earlier male emergence from hibernation may maintain protandry in this population, but did not contribute to further advances in male phenology. Together, our results provide evidence that the sexes should remain synchronized, at least in response to the weather variation investigated here, and further support the role of sexual selection in the evolution of protandry in sexually reproducing organisms.

Weathering the storm: Decreased activity and glucocorticoid levels in response to inclement weather in breeding Columbian ground squirrels.

Inclement weather can rapidly modify the thermal conditions experienced by animals, inducing changes in their behavior, body condition, and stress physiology, and affecting their survival and breeding success. For animals living in variable environments, the extent to which they have adapted to cope with inclement weather is not established, especially for hibernating species with a short active season that are constrained temporally to breed and store energy for subsequent hibernation. We examined behavioral (foraging activity) and physiological (body mass and fecal cortisol metabolites) responses of Columbian ground squirrels (Urocitellus columbianus), small hibernating rodents inhabiting open meadows in Rocky Mountains, to 3 events of inclement weather (two snow storms in May 2021 and May 2022, one heavy rainfall in June 2022). We found that individuals adapted to inclement weather conditions by (1) reducing above-ground activity, including foraging, (2) decreasing the mobilization of stored resources as indicated by a decrease in the activity of the hypothalamo-pituitary-adrenal (HPA) axis and lower fecal cortisol metabolites in the hours/days following periods of inclement weather; and (3) compensating through increased foraging and more local activity when favorable conditions resumed. As a result, body mass and growth did not decrease following short periods of inclement weather. Columbian ground squirrels were well-adapted to short periods of inclement weather, coping via modifications of their behavior and the activity of the HPA axis.

Effect of age on wingbeat frequency of Aedes aegypti and potential application for age estimation of mosquitoes.

To combat mosquito-borne diseases, a variety of vector control tools have been implemented. Estimating age structure in populations of vector species is important for understanding transmission potential. Age-grading techniques have been used as critical methods for evaluating the efficacy of vector control tools. However, methods like mark-release-recapture and ovarian dissection are laborious and require a high level of training. For decades, scientists have discussed the wide array of acoustic signatures of different mosquito species. These distinguishable wingbeat signatures with spatiotemporal classification allow mosquitoes of the same species to locate one another for mating. In recent years, the use of sensitive acoustic devices like mobile phones have proved effective. Wingbeat signatures can be used to identify mosquito species without the challenge of intensive field collections and morphological and molecular identifications. In this study, laboratory Aedes aegypti (L.) female and male wingbeats were recorded using mobile phones to determine whether sex and age differences with chronological time, and across different physiological stages, can be detected. Our results indicate significantly different wingbeat signatures between male and female Ae. aegypti, and a change of wingbeat frequencies with age and reproduction stage in females.

Two aspects of longevity are associated with rates of loss of telomeres in birds.

Telomeres, the terminal repetitive DNA sequences at the ends of linear chromosomes, have strong associations with longevity in some major taxa. Longevity has been linked to rate of decline in telomere length in birds and mammals, and absolute telomere length seems to be associated with body mass in mammals. Using a phylogenetic comparative method and 30 species of birds, we examined longevity (reflected by maximum lifespan), absolute telomere length, the rate of change in telomere length (TROC), and body mass (often strongly associated with longevity) to ascertain their degree of association. We divided lifespan into two life-history components, one reflected by body size (measured as body mass) and a component that was statistically independent of body mass. While both lifespan and body mass were strongly associated with a family tree of the species (viz., the phylogeny of the species), telomere measures were not. Telomere length was not significantly associated with longevity or body mass or our measure of mass-independent lifespan. TROC, however, was strongly associated with mass-independent lifespan, but only to a much lesser degree at best with body mass-predicted lifespan. Our results supported an association of TROC and longevity, in particular longevity that was independent of body size and part of the pace-of-life syndrome of life histories.

Effects of the social environment on vertebrate fitness and health in nature: Moving beyond the stress axis.

Social interactions are a ubiquitous feature of the lives of vertebrate species. These may be cooperative or competitive, and shape the dynamics of social systems, with profound effects on individual behavior, physiology, fitness, and health. On one hand, a wealth of studies on humans, laboratory animal models, and captive species have focused on understanding the relationships between social interactions and individual health within the context of disease and pathology. On the other, ecological studies are attempting an understanding of how social interactions shape individual phenotypes in the wild, and the consequences this entails in terms of adaptation. Whereas numerous studies in wild vertebrates have focused on the relationships between social environments and the stress axis, much remains to be done in understanding how socially-related activation of the stress axis coordinates other key physiological functions related to health. Here, we review the state of our current knowledge on the effects that social interactions may have on other markers of vertebrate fitness and health. Building upon complementary findings from the biomedical and ecological fields, we identify 6 key physiological functions (cellular metabolism, oxidative stress, cellular senescence, immunity, brain function, and the regulation of biological rhythms) which are intimately related to the stress axis, and likely directly affected by social interactions. Our goal is a holistic understanding of how social environments affect vertebrate fitness and health in the wild. Whereas both social interactions and social environments are recognized as important sources of phenotypic variation, their consequences on vertebrate fitness, and the adaptive nature of social-stress-induced phenotypes, remain unclear. Social flexibility, or the ability of an animal to change its social behavior with resulting changes in social systems in response to fluctuating environments, has emerged as a critical underlying factor that may buffer the beneficial and detrimental effects of social environments on vertebrate fitness and health.

Telomere dynamics in female Columbian ground squirrels: recovery after emergence and loss after reproduction.

Telomeres are specialized non-coding DNA sequences located at the end of chromosomes and that protect genetic information. Telomere loss over lifespan is generally viewed as a phenomenon associated with aging in animals. Recently, telomere elongation after hibernation has been described in several mammals. Whether this pattern is an adaptation to repair DNA damage caused during rewarming from torpor or if it coevolved as a mechanism to promote somatic maintenance in preparation for the upcoming reproductive effort remains unclear. In a longitudinal study measuring telomere length using buccal swabs, we tested if telomere elongation was related to reproductive success in wild adult female Columbian ground squirrels (Urocitellus columbianus) that were monitored from emergence from hibernation to the end of the reproductive season. We found three key results. First, female telomere length increased at the start of the breeding season, both in breeding and non-breeding individuals. Second, post-emergence telomere lengthening was unrelated to female future reproductive output. Third, telomere length decreased in breeding females during lactation, but remained stable in non-breeding females over a similar period. Within breeders, telomeres shortened more in females producing larger and heavier litters. We concluded that telomere lengthening after hibernation did not constrain immediate female reproductive capacities. It was more likely to be part of the body recovery process that takes place after hibernation. Telomere erosion that occurs after birth may constitute a physiological cost of female reproduction.

Territorial scent-marking effects on vigilance behavior, space use, and stress in female Columbian ground squirrels.

Social environments can profoundly affect the behavior and stress physiology of group-living animals. In many territorial species, territory owners advertise territorial boundaries to conspecifics by scent marking. Several studies have investigated the information that scent marks convey about donors' characteristics (e.g., dominance, age, sex, reproductive status), but less is known about whether scents affect the behavior and stress of recipients. We experimentally tested the hypothesis that scent marking may be a potent source of social stress in territorial species. We tested this hypothesis for Columbian ground squirrels (Urocitellus columbianus) during lactation, when territorial females defend individual nest-burrows against conspecifics. We exposed lactating females, on their territory, to the scent of other lactating females. Scents were either from unfamiliar females, kin relatives (a mother, daughter, or sister), or their own scent (control condition). We expected females to react strongly to novel scents from other females on their territory, displaying increased vigilance, and higher cortisol levels, indicative of behavioral and physiological stress. We further expected females to be more sensitive to unfamiliar female scents than to kin scents, given the matrilineal social structure of this species and known fitness benefits of co-breeding in female kin groups. Females were highly sensitive to intruder (both unfamiliar and kin) scents, but not to their own scent. Surprisingly, females reacted more strongly to the scent of close kin than to the scent of unfamiliar females. Vigilance behavior increased sharply in the presence of scents; this increase was more marked for kin than unfamiliar female scents, and was mirrored by a marked 131% increase in free plasma cortisol levels in the presence of kin (but not unfamiliar female) scents. Among kin scents, lactating females were more vigilant to the scent of sisters of equal age, but showed a marked 318% increase in plasma free cortisol levels in response to the scent of older and more dominant mothers. These results suggest that scent marks convey detailed information on the identity of intruders, directly affecting the stress axis of territory holders.

The influence of phylogeny and life history on telomere lengths and telomere rate of change among bird species: A meta-analysis.

Longevity is highly variable among animal species and has coevolved with other life-history traits, such as body size and rates of reproduction. Telomeres, through their erosion over time, are one of the cell mechanisms that produce senescence at the cell level and might even have an influence on the rate of aging in whole organisms. However, uneroded telomeres are also risk factors of cell immortalization. The associations of telomere lengths, their rate of change, and life-history traits independent of body size are largely underexplored for birds. To test associations of life-history traits and telomere dynamics, we conducted a phylogenetic meta-analysis using studies of 53 species of birds. We restricted analyses to studies that applied the telomere restriction fragment length (TRF) method, and examined relationships between mean telomere length at the chick (Chick TL) and adult (Adult TL) stages, the mean rate of change in telomere length during life (TROC), and life-history traits. We examined 3 principal components of 12 life-history variables that represented: body size (PC1), the slow-fast continuum of pace of life (PC2), and postfledging parental care (PC3). Phylogeny had at best a small-to-medium influence on Adult and Chick TL (r 2 = .190 and .138, respectively), but a substantial influence on TROC (r 2 = .688). Phylogeny strongly influenced life histories: PC1 (r 2 = .828), PC2 (.838), and PC3 (.613). Adult TL and Chick TL were poorly associated with the life-history variables. TROC, however, was negatively and moderate-to-strongly associated with PC2 (unadjusted r = -.340; with phylogenetic correction, r = -.490). Independent of body size, long-lived species with smaller clutches, and slower embryonic rate of growth may exhibit less change in telomere length over their lifetimes. We suggest that telomere lengths may have diverged, even among closely avian-related species, yet telomere dynamics are strongly linked to the pace of life.

Demographic responses to climate change in a threatened Arctic species.

The Arctic is undergoing rapid and accelerating change in response to global warming, altering biodiversity patterns, and ecosystem function across the region. For Arctic endemic species, our understanding of the consequences of such change remains limited. Spectacled eiders (Somateria fischeri), a large Arctic sea duck, use remote regions in the Bering Sea, Arctic Russia, and Alaska throughout the annual cycle making it difficult to conduct comprehensive surveys or demographic studies. Listed as Threatened under the U.S. Endangered Species Act, understanding the species response to climate change is critical for effective conservation policy and planning. Here, we developed an integrated population model to describe spectacled eider population dynamics using capture-mark-recapture, breeding population survey, nest survey, and environmental data collected between 1992 and 2014. Our intent was to estimate abundance, population growth, and demographic rates, and quantify how changes in the environment influenced population dynamics. Abundance of spectacled eiders breeding in western Alaska has increased since listing in 1993 and responded more strongly to annual variation in first-year survival than adult survival or productivity. We found both adult survival and nest success were highest in years following intermediate sea ice conditions during the wintering period, and both demographic rates declined when sea ice conditions were above or below average. In recent years, sea ice extent has reached new record lows and has remained below average throughout the winter for multiple years in a row. Sea ice persistence is expected to further decline in the Bering Sea. Our results indicate spectacled eiders may be vulnerable to climate change and the increasingly variable sea ice conditions throughout their wintering range with potentially deleterious effects on population dynamics. Importantly, we identified that different demographic rates responded similarly to changes in sea ice conditions, emphasizing the need for integrated analyses to understand population dynamics.

Parental investment in the Columbian ground squirrel: empirical tests of sex allocation models.

Parental allocation of resources into male or female offspring and differences in the balance of offspring sexes in natural populations are central research topics in evolutionary ecology. Fisher (Fisher, R. A. 1930. The genetical theory of natural selection, Clarendon Press, Oxford, UK) identified frequency-dependent selection as the mechanism responsible for an equal investment in the sexes of offspring at the end of parental care. Three main theories have been proposed for explaining departures from Fisherian sex ratios in light of variation in environmental (social) and individual (maternal condition) characteristics. The Trivers-Willard model (Trivers, R., and D. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90-92) of male-biased sex allocation by mothers in the best body condition is based on the competitive ability of male offspring for future access to mates and thus superior reproduction. The local resource competition model is based on competitive interactions in matrilines, as occur in many mammal species, where producing sons reduces future intrasexual competition with daughters. A final model invokes advantages of maintaining matrilines for philopatric females, despite any increased competition among females. We used 29 yr of pedigree and demographic data to evaluate these hypotheses in the Colombian ground squirrel (Urocitellus columbianus), a semisocial species characterized by strong female philopatry. Overall, male offspring were heavier than female offspring at birth and at weaning, suggesting a higher production cost. With more local kin present, mothers in the best condition biased their offspring sex ratio in favor of males, and mothers in poor condition biased offspring sex ratio in favor of females. Without co-breeding close kin, the pattern was reversed, with mothers in the best condition producing more daughters, and mothers in poor condition producing more sons. Our results do not provide strong support for any of the single-factor models of allocation to the sexes of offspring, but rather suggest combined influences of relative maternal condition and matriline dominance on offspring sex ratio.

Multiple paternity and the number of offspring: A model reveals two major groups of species.

Parentage analyses via microsatellite markers have revealed multiple paternity within the broods of polytocous species of mammals, reptiles, amphibians, fishes and invertebrates. The widespread phenomenon of multiple paternity may have attending relationships with such evolutionary processes as sexual selection and kin selection. However, just how much multiple paternity should a species exhibit? We developed Bayesian null models of how multiple paternity relates to brood sizes. For each of 114 species with published data on brood sizes and numbers of sires, we compared our null model estimates to published frequencies of multiple paternity. The majority of species fell close to our null model, especially among fish and invertebrate species. Some species, however, had low probabilities of multiple paternity, far from the predictions of the null model, likely due to sexual selection and environmental constraints. We suggest a major division among species' mating systems between those with close to random mating and high levels of multiple paternity, and those with constraints that produce low levels of multiple paternity.

Fluctuating optimum and temporally variable selection on breeding date in birds and mammals.

Temporal variation in natural selection is predicted to strongly impact the evolution and demography of natural populations, with consequences for the rate of adaptation, evolution of plasticity, and extinction risk. Most of the theory underlying these predictions assumes a moving optimum phenotype, with predictions expressed in terms of the temporal variance and autocorrelation of this optimum. However, empirical studies seldom estimate patterns of fluctuations of an optimum phenotype, precluding further progress in connecting theory with observations. To bridge this gap, we assess the evidence for temporal variation in selection on breeding date by modeling a fitness function with a fluctuating optimum, across 39 populations of 21 wild animals, one of the largest compilations of long-term datasets with individual measurements of trait and fitness components. We find compelling evidence for fluctuations in the fitness function, causing temporal variation in the magnitude, but not the direction of selection. However, fluctuations of the optimum phenotype need not directly translate into variation in selection gradients, because their impact can be buffered by partial tracking of the optimum by the mean phenotype. Analyzing individuals that reproduce in consecutive years, we find that plastic changes track movements of the optimum phenotype across years, especially in bird species, reducing temporal variation in directional selection. This suggests that phenological plasticity has evolved to cope with fluctuations in the optimum, despite their currently modest contribution to variation in selection.

Integrating Mortality Risk and the Adaptiveness of Hibernation.

Low mortality rate is often associated with slow life history, and so far, has mainly been assessed through examinations of specific adaptations and lifestyles that limit mortality risk. However, the organization of activity time budgets also needs to be considered, since some activities and the time afforded for performing them may expose animals to higher mortality risks such as increased predation and/or increased metabolic stress. We examined the extent of activity time budgets contribution to explaining variation in life history traits in mammals. We specifically focused on hibernating species because of their marked seasonal cycle of activity/inactivity associated with very different mortality risks. Hibernation is considered a seasonal adaptation to prolonged periods of food shortage and cold. This inactivity period may also reduce both extrinsic and intrinsic mortality risks, by decreasing exposure to predators and drastically reducing metabolic rate. In turn, reduction in mortality may explain why hibernators have slower life history traits than non-hibernators of the same size. Using phylogenetically controlled models, we tested the hypothesis that longevity was positively correlated with the hibernation season duration (the time spent between immergence and emergence from the hibernaculum or den) across 82 different mammalian species. We found that longevity increased significantly with hibernation season duration, an effect that was particularly strong in small hibernators (<1.5 kg) especially for bats. These results confirm that hibernation not only allows mammals to survive periods of energy scarcity, but further suggest that activity time budgets may be selected to reduce mortality risks according to life history pace.

Estimating a Key Parameter of Mammalian Mating Systems: The Chance of Siring Success for a Mated Male.

Studies of multiple paternity in mammals and other animal species generally report proportion of multiple paternity among litters, mean litter sizes, and mean number of sires per litter. It is shown how these variables can be used to produce an estimate of the probability of reproductive success for a male that has mated with a female. This estimate of male success is more informative about the mating system that alternative measures, like the proportion of litters with multiple paternity or the mean number of sires per litter. The probability of success for a mated male can be measured both theoretically and empirically, and gives an estimate of the intensity of sperm competition and of a male's "confidence of paternity" upon mating. The probability of success for mated males for ten "exemplar" species of mammals is estimated and they are compared for insights into the functioning of their mating systems.

Subtle short-term physiological costs of an experimental augmentation of fleas in wild Columbian ground squirrels.

Parasites affect many aspects of host physiology and behavior, and thus are generally thought to negatively impact host fitness. However, changes in form of short-term parasite effects on host physiological markers have generally been overlooked in favor of fitness measures. Here, we studied flea (Oropsylla idahoensis and Oropsylla opisocroistis tuberculata) parasitism on a natural population of Columbian ground squirrels (Urocitellus columbianus) in Sheep River Provincial Park, AB, Canada. Fleas were experimentally added to adult female U. columbianus at physiologically demanding times, including birth, lactation and weaning of their young. The body mass of adult females, as well as their oxidative stress and immunity were recorded multiple times over the active season under flea-augmented and control conditions. We also measured the prevalence of an internal parasite (Trypanosoma otospermophili). Doubly labeled water (DLW) was intra-peritoneally injected at peak lactation to examine energy expenditure. Effects of parasites on oxidative stress were only observed after offspring were weaned. There was no direct effect of experimentally heightened flea prevalence on energy use. A short-term 24 h mass loss (-17 g) was detected briefly after parasite addition, likely due to U. columbianus preferentially allocating time for grooming. Our parasite augmentation did not strongly affect hosts and suggested that short-term physiological effects were unlikely to culminate in long-term fitness consequences. Columbian ground squirrels appear to rapidly manage parasite costs, probably through grooming.