Biology subjects

McAdam, A. G.

Publications and source records attributed to McAdam, A. G..

At least 19 recordsLinked to original sources

bioRxiv2026

Maternal effects shape scale-dependent convergence in gut microbial responses to environmental change

Animals can experience environmental variability across multiple temporal scales, from predictable within-year seasonal fluctuations to rarer, irregular resource pulses that occur across generations. While gut microbiome responses to seasonal changes are well documented, far less is understood about how host-associated microbiomes respond to episodic environmental resource pulses, and whether such responses can persist across generations. Here, we investigate how gut microbial communities of wild North American red squirrels (Tamiasciurus hudsonicus) respond to intra-annual seasonal variation and episodic resource pulses happening years apart (specifically, seed masting). We then test the hypothesis that these responses are shared by mothers and their offspring. In line with prior work across mammals, we found that seasonal variation strongly structured gut microbiomes, driving widespread and convergent shifts in composition across the year. However, episodic resource pulses predicted microbial scatter such that gut microbiomes became more dissimilar across individuals in resource pulse years compared to typical years. Despite this population-level divergence, mothers and their adult offspring exhibited microbial convergence when encountering resource pulses occurring years apart, whereas seasonal responses were shared across the population and not unique to mother-offspring pairs. Overall, our results highlight the mammalian gut microbiome as a flexible component of the host phenotype, capable of adjusting to both predictable seasonal variation and large-scale, episodic resource pulses. Patterns of mother-offspring similarity across resource pulse years further provide evidence that some host-microbial responses to environmental change may be transmitted across generations.

ecology↗

bioRxiv2025

Developmental conditions shape lifetime reproductive strategies in a wild mammal

Coping with developmental hardship is a defining feature of resilience across the tree of life. Compensatory strategies that preserve fitness after a poor start are hypothesized to be favored by natural selection, but empirical evidence is rare. Using over three decades of data on >1,000 reproductive attempts across the lifetimes of 405 wild female red squirrels, we show that developmental adversity prompts adaptive reorganization of reproductive investment across the lifespan. Hardships reduced lifetime reproductive opportunities, but triggered opposing strategies. Extrinsic mortality risk predicted frontloading of reproduction at debut, while poor maternal investment predicted terminal reproductive effort at a cost to future generations. Both strategies preserved lifetime fitness, revealing how context-dependent reproductive plasticity over the life course can rescue the fitness consequences of developmental hardship.

ecology↗

bioRxiv2024

Territorial behavior as a route of social microbial transmission in an asocial mammal

Microbial transmission is a major benefit of sociality, facilitated by affiliative behaviors such as grooming and communal nesting in group-living animals. The spread of microbial symbionts through these pathways, and their incorporation into host microbiomes, can enhance host health and fitness by contributing to pathogen protection and metabolic flexibility. Are pathways that facilitate microbial transfer across hosts also present in animals that do not form social groups because territoriality limits social interactions and prevents group formation? Here, we addressed this question by combining longitudinal sampling of individual gut microbial communities, demographic data, and dynamic behavioral and spatial measures of territoriality from a non-social, highly territorial small mammal: wild North American red squirrels (Tamiasciurus hudsonicus). As squirrel densities increased, individual gut microbial communities became richer and more phylogenetically diverse, while among-individual differences in composition decreased. This pattern was characterized primarily by increases in obligately anaerobic and non-sporulating taxa with little to no tolerance for oxygen-rich environments, suggesting social rather than environmental routes of transmission. Moreover, territorial intrusions--in which conspecifics were found on within an individuals territorial space--increased gut microbial diversity among individuals defending larger territorial spaces. Using an intrusion-based social network analysis, we found that that pairs with stronger social association (via intrusions) exhibited higher gut microbial similarity. Taken together, our findings provide some of the first evidence for social microbial transmission in a non-social species, and suggest that increased density and territorial behavior can diversify and homogenize host gut microbial communities despite social isolation.

ecology↗

bioRxiv2024

Timing-dependent effects of elevated maternal glucocorticoids on offspring brain gene expression in a wild small mammal

An increase in maternal stress during offspring development can have cascading, life-long impacts on offspring behavior and physiology, which can vary depending on the timing of exposure to the stressor. By responding to stressors through increasing production of glucocorticoids (GCs), the hypothalamic-pituitary-adrenal (HPA) axis is a key mediator of maternal effects - both on the side of the mother and the offspring. At a molecular level, maternal effects are thought to be mediated through modifying transcription of genes, particularly in the brain. To better understand the evolutionary implications of maternal effects, more studies are needed on mechanisms of maternal effects in wild populations. To test how the timing of maternal stress impacts gene expression in the brains of offspring, we treated free-ranging North American red squirrels (Tamiasciurus hudsonicus) with GCs during late pregnancy or early lactation and collected brains from offspring around weaning. We used RNA-sequencing to measure gene expression in the hypothalamus and hippocampus. We found small differences in gene expression between GC-treated and control individuals suggesting long-term effects of the GC treatment on neural gene transcription. The general patterns of gene regulation across the transcriptome were consistent between the pregnancy and lactation-treated individuals. However, the number of significantly differentially expressed genes was higher in the lactation treatment group. These results support the idea that maternal stress affects neural gene expression in offspring, and these effects are dependent on timing. Our findings add valuable insight into the impact of maternal hormones on neural transcriptomics in a wild population.

ecology↗

bioRxiv2023

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

Adverse early-life conditions, even when transient, can have long-lasting effects on individual phenotypes and reduce lifespan across species. If these effects can be mitigated. by a high quality later-life environment, then differences in future resource access may explain variation in vulnerability and resilience to early-life adversity. Using 32 years of data on 1,000+ wild North American red squirrels, we tested the hypothesis that the negative effects of early-life adversity on lifespan can be buffered by later-life food abundance. We found that although cumulative early-life adversity was negatively associated with adult lifespan, this relationship was modified by future food abundance. Squirrels that experienced a naturally-occurring future food boom in the second year of life did not suffer reduced longevity despite early-life adversity. Experimental supplementation with additional food did not replicate this effect, though it did increase adult lifespan overall. Our results suggest a non-deterministic role for early-life conditions on later-life phenotypes, and highlight the importance of contextualizing the influence of harsh early-life conditions over an animals entire life course.

evolutionary biology↗

bioRxiv2023

Interpretation of body condition index should be informed by natural history

Many studies assume that it is beneficial for individuals of a species to be heavier, or have a higher body condition index (BCI), without accounting for the physiological relevance of variation in the composition of different body tissues. We hypothesized that the relationship between BCI and masses of physiologically important tissues (fat and lean) would be conditional on annual patterns of energy acquisition and expenditure. We studied 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 adults of both sexes using quantitative magnetic resonance (QMR). We measured body mass and 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). In all cases, however, BCI was never better than body mass alone in predicting fat or lean mass. While the accuracy of BCI in estimating fat varied across the natural histories and annual energetic patterns of the species considered, measuring body mass alone was as effective, or superior in capturing sufficient variation in fat and lean in most cases.

physiology↗

bioRxiv2021

Benefits of living closer to kin vary by genealogical relationship in a territorial mammal

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 geographic 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.

animal behavior and cognition↗

bioRxiv2021

Using a Homeogram to Detect Sleep in Free-living Animals

O_LISleep 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. C_LIO_LIWe 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. C_LIO_LIOur 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. C_LIO_LIApplying our analytical strategy to accelerometer data from other species may open new possibilities to investigate sleep patterns for researchers studying wild animals. C_LI

animal behavior and cognition↗

bioRxiv2020

Maternal glucocorticoids do not influence HPA axis activity or behavior of juvenile wild North American red squirrels

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.

animal behavior and cognition↗

bioRxiv2020

Examining interspecific density-dependent dispersal in forest small mammals

The effects of conspecific densities on dispersal have been well documented. However, while positive and negative density-dependent dispersal based on conspecific densities are often shown to be the result of intraspecific competition or facilitation respectively, the effects of heterospecific densities on dispersal are examined far less frequently. This despite the potential for the analogous processes of interspecific competition and heterospecific attraction to influence dispersal. Here we use 51 years of live-trapping data on deer mouse (Peromsycus maniculatus), eastern chipmunk (Tamias striatus), red-backed vole (Myodes gapperi), and jumping mice (Napaeozapus insignis and Zapus hudsonius) to examine the effects of both conspecific and heterospecific densities on dispersal frequency. In terms of conspecific densities, jumping mice were more likely to disperse from areas of low conspecific densities, while red-backed voles and chipmunks did not respond to conspecific densities in their dispersal frequencies. When considering interspecific density effects, while there were no statistically clear effects of density on dispersal frequency, the effects of chipmunk and jumping mice densities on dispersal by red-backed vole were greater than the effects of conspecific densities, with voles more likely to disperse from areas of high chipmunk densities and low jumping mice densities. Likewise, the effect of chipmunk densities on dispersal by jumping mice was greater than the conspecific density effect. Conspecific densities clearly can affect dispersal by two of these four species, but the effects of heterospecific densities on dispersal frequency are less clear. Based on effect sizes it appears that there is potential for heterospecific effects on dispersal by some species in the community, but future experimental work could elucidate the strength and causes of these relationships.

ecology↗

bioRxiv2019

Maternal stress promotes offspring growth without oxidative costs in wild red squirrels

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.

evolutionary biology↗

bioRxiv2019

Territory acquisition mediates the influence of predators and climate on juvenile red squirrel survival

1) Juvenile survival to first breeding is a key life history stage. Survival through this period can be particularly challenging when it coincides with harsh environmental conditions like winter climate or food scarcity, and so cohort survival can be highly variable. However, the small size and dispersive nature of juveniles makes studying their survival difficult.\n2) In territorial species, a key life history event is the acquisition of a territory. A territory is expected to enhance survival, but how it does so, possibly through mediating mortality, is not often identified. We tested how the timing of territory acquisition influenced the survival of juvenile North American red squirrels Tamiasciurus hudsonicus, hereafter red squirrels, and how the timing of this event mediated sources of mortality. We hypothesized that securing a territory prior to the caching season would reduce juvenile susceptibility to predation or climatic factors over winter.\n3) Using 27 years of data on the survival of individually-marked juvenile red squirrels, we tested how the timing of territory acquisition influenced survival, whether the population density of red squirrel predators and mean temperature over winter were related to individual survival probability, and if territory ownership mediated these effects.\n4) Juvenile survival was lower in years of high predator abundance and in colder winters. Autumn territory owners were less susceptible to lynx Lynx canadensis, and possibly mustelid Mustela and Martes spp., predation. Autumn territory owners had lower survival in colder winters, while non-owners had higher survival in cold winters.\n5) Our results show how the timing of a life history event like territory acquisition can directly affect survival and also mediate the effects of biotic and abiotic factors later in life. This engenders a better understanding of the fitness consequences of the timing of key life history events.

ecology↗

bioRxiv2019

Fitness benefits of a motivated mom

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 behavior 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 behavior can alter a fundamental life history trade-off between offspring quantity and quality.\n\nLay SummaryIt 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 observed repeatable individual variation in maternal attentiveness towards offspring. 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 recruit into the breeding population.

evolutionary biology↗

bioRxiv2019

Familiar neighbors, but not relatives, enhance fitness in a territorial mammal

SummaryOne of the outstanding questions in evolutionary biology is the extent to which mutually beneficial interactions and kin-selection can facilitate the evolution of cooperation by mitigating conflict between interacting organisms. The indirect fitness benefits gained from associating with kin are an important pathway to conflict resolution [1], but conflict can also be resolved if individuals gain direct benefits from cooperating with one another (e.g. mutualism or reciprocity) [2]. Owing to the kin-structured nature of many animal societies, it has been difficult for previous research to assess the relative importance of these mechanisms [3-5]. However, one area that might allow for the relative roles of kin-selection and mutualistic benefits to be disentangled is in the resolution of conflict over territorial space [6]. While much research has focused on group-living species, the question of how cooperation can first be favoured in solitary, territorial species remains a key question. Using 22 years of data from a population of North American red squirrels, we assessed how kinship and familiarity with neighbours affected fitness in a territorial mammal. While living near kin did not enhance fitness, familiarity with neighbours increased survival and annual reproductive success. These fitness benefits were strong enough to compensate for the effects of aging later in life, with potential consequences for the evolution of senescence. We suggest that such substantial fitness benefits provide the opportunity for the evolution of cooperation between adversarial neighbours, offering insight into the role that mutually beneficial behaviours might play in facilitating and stabilizing social systems. Graphical Abstract O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY C_FIG_DISPLAY

evolutionary biology↗

bioRxiv2019

Variation in space and time: a long-term examination of density-dependent dispersal in a woodland rodent

Dispersal is a fundamental ecological process that can be affected by population density, yet studies report contrasting effects of density on propensity to disperse. Additionally, the relationship between dispersal and density is seldom examined using densities measured at different spatial scales or over extensive time-series. We used 51-years of trapping data to examine how dispersal by wild deer mice (Peromyscus maniculatus) was affected by changes in both local and regional population densities. We examined these patterns over both the entire time-series and also in ten-year shifting windows to determine whether the nature and strength of the relationship changed through time. Probability of dispersal decreased with increased local and regional population density, and the negative effect of local density on dispersal was more pronounced in years with low regional densities. Additionally, the strength of negative density-dependent dispersal changed through time, ranging from very strong in some decades to absent in other periods of the study. Finally, while females were less likely to disperse, female dispersal was more density-dependent than male dispersal. Our study shows that the relationship between density and dispersal is not temporally static and that investigations of density-dependent dispersal should consider both local and regional population densities.

ecology↗

bioRxiv2018

Is physiological stress state reflected in acoustic structure of vocalizations? An experimental test in wild North American red squirrels

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, very few studies have experimentally examined the acoustic expression of short-term stress state. The transmission of such information about physiological state could have broad implications, potentially allowing other individuals to modify their behavior or life history traits in response to this public information. 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. Our results provide mixed evidence that rattles show 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 received control treatments and unmanipulated (unfed) squirrels. Our results indicate that short-term stress does affect the acoustic structure of vocalizations, but elevated circulating GC levels are not solely responsible for such changes.

animal behavior and cognition↗

bioRxiv2018

Indirect genetic effects clarify how traits can evolve even when fitness does not

There are many situations in nature where we expect traits to evolve but not necessarily for mean fitness to increase. However, these scenarios are hard to reconcile simultaneously with Fishers Fundamental Theorem of Natural Selection and the Price identity. The consideration of indirect genetic effects on fitness reconciles these fundamental theorems with the observation that traits sometimes evolve without any adaptation, by explicitly considering the correlated evolution of the social environment, which is a form of transmission bias. While transmission bias in the Price identity is often assumed to be absent, here we show that explicitly considering indirect genetic effects as a form of transmission bias for fitness has several benefits: 1) it makes clear how traits can evolve while mean fitness remains stationary, 2) it reconciles the fundamental theorem of natural selection with the evolution of maladaptation, 3) it explicitly includes density-dependent fitness through negative social effects that depend on the number of interacting conspecifics, and 4) its allows mean fitness to evolve even when direct genetic variance in fitness is zero, if related individuals interact and/or if there is multilevel selection. In summary, considering fitness in the context of indirect genetic effects aligns important theorems of natural selection with many situations observed in nature and provides a useful lens through which we might better understand evolution and adaptation.

evolutionary biology↗

bioRxiv2018

Red squirrels mitigate costs of territory defence through social plasticity

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) were 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. Long-term 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 was 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 can reduce the costs of territoriality by appropriately adjusting behaviour in response to changes in their social environment. 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.

animal behavior and cognition↗