Biology subjects

Lane, J. E.

Publications and source records attributed to Lane, J. E..

17 recordsLinked to original sources

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↗

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↗

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↗

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

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↗

bioRxiv2018

Red squirrel territorial vocalizations deter intrusions by conspecific rivals

In many species, territory defense is thought to be one of the primary functions of acoustic communication. North American red squirrels are a territorial species in which rattles have long been thought to be the principal signal communicating territory ownership. These vocalizations have been assumed to deter intruders, thus reducing energy costs and the risk of injury associated with direct aggressive interactions. However, this hypothesis has not been directly tested. Here we used a speaker occupation experiment to test whether red squirrel rattles function to deter conspecific rivals. We studied 29 male squirrels and removed each individual from his territory twice in a paired design. During the experimental treatment we simulated the owners presence after its removal by broadcasting the owners rattle from a loudspeaker at the center of the territory once every seven minutes. During the control treatment the territory was left in silence after the temporary removal of the owner. We found that the presence of a speaker replacement reduced the probability of intrusion by 34% and increased the latency to first intrusion by 7%, providing support for the hypothesis that rattles play an active role in reducing intrusion risk. However, intrusions were not completely averted by the speaker replacement, indicating that vocalizations alone are not sufficient without other cues of the territory owner.

animal behavior and cognition↗

bioRxiv2018

Individual variation in the dear enemy phenomenon via territorial vocalizations in red squirrels

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 (n = 41) 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.

animal behavior and cognition↗

bioRxiv2018

Indirect effects on fitness between individuals that have never met via an extended phenotype

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 which mean the environments others experience are altered. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is almost always inherited by non relatives. Hoarding by previous owners can therefore influence subsequent owners. We found that red squirrels bred earlier and had higher lifetime fitness if the previous 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 others resource dependent traits and fitness without meeting via extended phenotypes, and so the past can influence contemporary population dynamics.

ecology↗

bioRxiv2018

Indirect effects of territorial neighbors on the timing of spring breeding may counteract changes in selection in North American red squirrels

Organisms can affect one anothers phenotypes when they socially interact. Indirect genetic effects occur when an individuals 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 variance parameters and the strength of selection at low and high population densities. Social effects of neighbours on the date of spring breeding were weak at low, but stronger at high population densities. Indirect phenotypic effects accounted for a larger amount of variation in the date of breeding than direct differences among-individuals, although the genetic component to these indirect effects was not statistically significant. Nevertheless, the estimated effect size was large enough to suggest that indirect genetic effects could alter evolutionary change, resulting in less change at high densities despite stronger selection. Despite the difficulty in estimating them precisely, indirect genetic effects have clear potential to alter evolutionary trajectories in any natural systems where organisms interact.

evolutionary biology↗

bioRxiv2018

Experimental increases in glucocorticoids alter function of the neuroendocrine stress axis in wild red squirrels without negatively impacting survival and reproduction

Hormones such as glucocorticoids (colloquially referred to as "stress hormones") have important effects on animal behavior and life history traits, yet most of this understanding has come through correlative studies. While experimental studies offer the ability to assign causality, there are important methodological concerns that are often not considered when manipulating hormones, including glucocorticoids, in wild animals. In this study, we examined how experimental elevations of cortisol concentrations in wild North American red squirrels (Tamiasciurus hudsonicus) affected their hypothalamic-pituitary-adrenal (HPA) axis reactivity, and life history traits including body mass, litter survival, and adult survival. The effects of exogenous cortisol on plasma cortisol concentrations depended on the time between treatment consumption and blood sampling. In the first nine hours after consumption of exogenous cortisol, individuals had significantly higher true baseline plasma cortisol concentrations, but adrenal gland function was impaired as indicated by their dampened response to capture and handling and to injections of adrenocorticotropic hormone compared to controls. Approximately 24 hours after consumption of exogenous cortisol, individuals had much lower plasma cortisol concentrations than controls, but adrenal function was restored. Corticosteroid binding globulin (CBG) concentrations were also significantly reduced in squirrels treated with cortisol. Despite these profound shifts in the functionality of the HPA axis, squirrel body mass, offspring survival, and adult survival were unaffected by experimental increases in cortisol concentrations. Our results highlight that even short-term experimental increases in glucocorticoids can affect adrenal gland functioning and CBG concentrations but without other side-effects.

zoology↗

bioRxiv2017

Multilevel And Sex-Specific Selection On Competitive Traits In North American Red Squirrels

Individuals often interact more closely with some members of the population (e.g. offspring, siblings or group members) than they do with other individuals. This structuring of interactions can lead to multilevel natural selection, where traits expressed at the group-level influence fitness alongside individual-level traits. Such multilevel selection can alter evolutionary trajectories, yet is rarely quantified in the wild, especially for species that do not interact in clearly demarcated groups. We quantified multilevel natural selection on two traits, postnatal growth rate and birth date, in a population of North American red squirrels (Tamiasciurus hudsonicus). The strongest level of selection was typically within-acoustic social neighbourhoods (within 130m of the nest), where growing faster and being born earlier than nearby litters was key, while selection on growth rate was also apparent both within-litters and within-study areas. Higher population densities increased the strength of selection for earlier breeding, but did not influence selection on growth rates. Females experienced especially strong selection on growth rate at the within-litter level, possibly linked to the biased bequeathal of the maternal territory to daughters. Our results demonstrate the importance of considering multilevel and sex-specific selection in wild species, including those that are territorial and sexually monomorphic.\n\nData archival: the data set is archived on Dryad (info XXX), with a five-year embargo from the date of publication.

evolutionary biology↗