Evolutionary lability of food caching behaviour in mammals.

Food hoarding provides animals access to resources during periods of scarcity. Studies on mammalian caching indicate associations with brain size, seasonality and diet but are biased to a subset of rodents. Whether the behaviour is generalizable at other taxonomic scales and/or is influenced by other ecological factors is less understood. Population density may influence food caching due to food competition or pilferage, but this remains untested in a comparative framework. Using phylogenetic analyses, we assessed the role of morphology (body and brain size), climate, diet breadth and population density on food caching behaviour evolution at multiple taxonomic scales. We also used a long-term dataset on caching behaviour of red squirrels (Tamiasciurus fremonti) to test key factors (climate and population density) on hoarding intensity. Consistent with previous smaller scale studies, we found the mammalian ancestral state for food caching was larderhoarding, and scatterhoarding was derived. Caching strategy was strongly associated with brain size, population density and climate. Mammals with larger brains and hippocampal volumes were more likely to scatterhoard, and species living at higher population densities and in colder climates were more likely to larderhoard. Finer-scale analyses within families, sub-families and tribes indicated that the behaviour is evolutionary labile. Brain size in family Sciuridae and tribe Marmotini was larger in scatterhoarders, but not in other tribes. Scatterhoarding in tribe Marmotini was more likely in species with lower population densities while scatterhoarding in tribe Sciurini was associated with warmer climates. Red squirrel larderhoarding intensity was positively related to population density but not climate, implicating food competition or pilferage as an important mechanism mediating caching behaviour. Our results are consistent with previous smaller-scale studies on food caching and indicate the evolutionary patterns of mammalian food caching are broadly generalizable. Given the lability of caching behaviour as evidenced by the variability of our results at finer phylogenetic scales, comparative analyses must consider taxonomic scale. Applying our results to conservation could prove useful as changes in population density or climate may select for different food caching strategies and thus can inform management of threatened and endangered species and their habitats.

Inferring condition in wild mammals: body condition indices confer no benefit over measuring body mass across ecological contexts.

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.

Multiple cache recovery task cannot determine memory mechanisms.

A recent paper Smulders et al., (2023) analyzed results of an experiment in which food-caching coal tits needed to relocate and recover multiple previously made food caches and argued that food caching parids use familiarity and not recollection memory when recovering food caches. The memory task involving recovery of multiple caches in the same trial, however, cannot discriminate between these two memory mechanisms because small birds do not need to recover multiple caches to eat during a single trial. They satiate quickly after eating just the first recovered food cache and quickly lose motivation to search for caches, and can be expected to start exploring noncache locations rather than recovering the remaining caches, which would result in inaccurate memory measurements.

Natural variation in developmental condition has limited effect on spatial cognition in a wild food-caching bird.

Laboratory studies show that increased physiological burden during development results in cognitive impairment. In the wild, animals experience a wide range of developmental conditions, and it is critical to understand how variation in such conditions affects cognitive abilities later in life, especially in species that strongly depend on such abilities for survival. We tested whether variation in developmental condition is associated with differences in spatial cognitive abilities in wild food-caching mountain chickadees. Using tail feathers grown during development in juvenile birds, we measured feather corticosterone (Cortf) levels and growth rates and tested these birds during their first winter on two spatial learning tasks. In only 1 of the 3 years, higher feather Cortf was negatively associated with memory acquisition. No significant associations between feather Cortf and any other measurement of spatial cognition were detected in the other 2 years of the study or between feather growth rate and any measurement of cognition during the entire study. Our results suggest that in the wild, naturally existing variation in developmental condition has only a limited effect on spatial cognitive abilities, at least in a food-caching species. This suggests that there may be compensatory mechanisms to buffer specialized cognitive abilities against developmental perturbations.

Canada jays (Perisoreus canadensis) balance protein and energy targets simultaneously in both consumed and cached food.

Food scarce periods pose serious physiological challenges for birds, especially in energetically demanding conditions. For species in the northern hemisphere, a decrease in available resources during winter adds further physiological stress to the energetic demands of life at low temperatures. Some species cache food to provide a reliable energy and nutrient resource during scarcity. Canada Jays are a year-round food-caching resident of the North American boreal forest. Canada Jays also rear their young prior to spring green up, making food caching not only essential for adult winter survival, but also potentially important for meeting the requirements of growing offspring in late winter and early spring. We examined the diet choices of Canada Jays immediately prior to winter, and the macronutrient composition of the foods Canada Jay consumed and cached at this time. We found that Canada Jays cache the same relative amounts of macronutrients as they consume but did not vary macronutrients seasonally. The similarities in the macronutrient proportions cached and consumed suggest a consistent nutrient intake pattern, and that Canada Jays are foraging to simultaneously meet similar minimum energy and minimum protein targets for both the present and future. These simultaneous targets constrain the caching decisions of jays when presented with dietary choices.

Specialized spatial cognition is associated with reduced cognitive senescence in a food-caching bird.

Senescence, the gradual reduction and loss of function as organisms age, is a widespread process that is especially pronounced in cognitive abilities. Senescence appears to have a genetic basis and can be affected by evolutionary processes. If cognitive senescence is shaped by natural selection, it may be linked with selection on cognitive abilities needed for survival and reproduction, such that species where fitness is directly related to cognitive abilities should evolve delayed cognitive senescence likely resulting in higher lifetime fitness. We used wild food-caching mountain chickadees, which rely on specialized spatial cognition to recover thousands of food caches annually, to test for cognitive senescence in spatial learning and memory and reversal spatial learning and memory abilities. We detected no signs of age-related senescence in spatial cognitive performance on either task in birds ranging from 1 to 6 years old; older birds actually performed better on spatial learning and memory tasks. Our results therefore suggest that cognitive senescence may be either delayed (potentially appearing after 6 years) or negligible in species with strong selection on cognitive abilities and that food-caching species may present a useful model to investigate mechanisms associated with cognitive senescence.

Food discovery is associated with different reliance on social learning and lower cognitive flexibility across environments in a food-caching bird.

Social learning is a primary mechanism for information acquisition in social species. Despite many benefits, social learning may be disadvantageous when independent learning is more efficient. For example, searching independently may be more advantageous when food sources are ephemeral and unpredictable. Individual differences in cognitive abilities can also be expected to influence social information use. Specifically, better spatial memory can make a given environment more predictable for an individual by allowing it to better track food sources. We investigated how resident food-caching chickadees discovered multiple novel food sources in both harsher, less predictable high elevation and milder, more predictable low elevation winter environments. Chickadees at high elevation were faster at discovering multiple novel food sources and discovered more food sources than birds at low elevation. While birds at both elevations used social information, the contribution of social learning to food discovery was significantly lower at high elevation. At both elevations, chickadees with better spatial cognitive flexibility were slower at discovering food sources, likely because birds with lower spatial cognitive flexibility are worse at tracking natural resources and therefore spend more time exploring. Overall, our study supported the prediction that harsh environments should favour less reliance on social learning.

Social dominance has limited effects on spatial cognition in a wild food-caching bird.

Social dominance has long been used as a model to investigate social stress. However, many studies using such comparisons have been performed in captive environments. These environments may produce unnaturally high antagonistic interactions, exaggerating the stress of social subordination and any associated adverse consequences. One such adverse effect concerns impaired cognitive ability, often thought to be associated with social subordination. Here, we tested whether social dominance rank is associated with differences in spatial learning and memory, and in reversal spatial learning (flexibility) abilities in wild food-caching mountain chickadees at different montane elevations. Higher dominance rank was associated with higher spatial cognitive flexibility in harsh environments at higher elevations, but not at lower, milder elevations. By contrast, there were no consistent differences in spatial learning and memory ability associated with dominance rank. Our results suggest that spatial learning and memory ability in specialized food-caching species is a stable trait resilient to social influences. Spatial cognitive flexibility, on the other hand, appears to be more sensitive to environmental influences, including social dominance. These findings contradict those from laboratory studies and suggest that it is critical to investigate the biological consequences of social dominance under natural conditions.

Testing the greater male variability phenomenon: male mountain chickadees exhibit larger variation in reversal learning performance compared with females.

The greater male variability phenomenon predicts that males exhibit larger ranges of variation in cognitive performance compared with females; however, support for this pattern has come exclusively from studies of humans and lacks mechanistic explanation. Furthermore, the vast majority of the literature assessing sex differences in cognition is based on studies of humans and a few other mammals. In order to elucidate the underpinnings of cognitive variation and the potential for fitness consequences, we must investigate sex differences in cognition in non-mammalian systems as well. Here, we assess the performance of male and female food-caching birds on a spatial learning and memory task and a reversal spatial task to address whether there are sex differences in mean cognitive performance or in the range of variation in performance. For both tasks, male and female mean performance was similar across four years of testing; however, males did exhibit a wider range of variation in performance on the reversal spatial task compared with females. The implications for mate choice and sexual selection of cognitive abilities are discussed and future directions are suggested to aid in the understanding of sex-related cognitive variation.

Smart is the new sexy: female mountain chickadees increase reproductive investment when mated to males with better spatial cognition.

Understanding the evolution of inter and intraspecific variation in cognitive abilities is one of the main goals in cognitive ecology. In scatter-caching species, spatial memory is critical for the recovery of food caches and overwinter survival, but its effects on reproduction are less clear. Better spatial cognition may improve pre-breeding condition allowing for earlier reproduction. Alternatively, when mated to males with better spatial memory, females may be able to invest more in reproduction which may allow increased offspring survival and hence higher fitness. Using wild food-caching mountain chickadees, we found that when environmental conditions were favourable for breeding, females mated to males with better spatial cognition laid larger clutches and fledged larger broods than females mated to males with worse cognitive performance. Our results support the hypothesis that females may increase their reproductive investment to gain indirect, genetic benefits when mated to high-quality males with better spatial cognitive abilities.

What makes specialized food-caching mountain chickadees successful city slickers?

Anthropogenic environments are a dominant feature of the modern world; therefore, understanding which traits allow animals to succeed in these urban environments is especially important. Overall, generalist species are thought to be most successful in urban environments, with better general cognition and less neophobia as suggested critical traits. It is less clear, however, which traits would be favoured in urban environments in highly specialized species. Here, we compared highly specialized food-caching mountain chickadees living in an urban environment (Reno, NV, USA) with those living in their natural environment to investigate what makes this species successful in the city. Using a 'common garden' paradigm, we found that urban mountain chickadees tended to explore a novel environment faster and moved more frequently, were better at novel problem-solving, had better long-term spatial memory retention and had a larger telencephalon volume compared with forest chickadees. There were no significant differences between urban and forest chickadees in neophobia, food-caching rates, spatial memory acquisition, hippocampus volume, or the total number of hippocampal neurons. Our results partially support the idea that some traits associated with behavioural flexibility and innovation are associated with successful establishment in urban environments, but differences in long-term spatial memory retention suggest that even this trait specialized for food-caching may be advantageous. Our results highlight the importance of environmental context, species biology, and temporal aspects of invasion in understanding how urban environments are associated with behavioural and cognitive phenotypes and suggest that there is likely no one suite of traits that makes urban animals successful.

The maturation of research into the avian hippocampal formation: Recent discoveries from one of the nature's foremost navigators.

For more than 30 years, a growing number of researchers have been attracted to the challenge of understanding the neurobiological organization of the avian hippocampal formation (HF) and its relationship to the remarkable spatial cognitive abilities of birds. In this selective review, we highlight recent anatomical and developmental findings that reveal a HF design that defies any simple comparison to the mammalian hippocampus and leaves unanswered the seemingly enduring question of whether a dentate gyrus homologue is to be found in HF. From a functional perspective, we highlight the recent discoveries that implicate HF in the use of space for memory pattern segregation and continued interest in the role HF neurogenesis may play in supporting memory function and its relationship to memory decline in aging birds. We also summarize data that nurture a fundamental reinterpretation of the role of HF in spatial cognition by suggesting HF involvement in spatial perception antecedent to any memory formation. Given the disproportionate adaptive significance of space for birds, which has led to the evolution of their exceptional navigational and memory abilities, there is little doubt that the avian HF will continue to provide important and unexpected insights into the neural basis of spatial cognition.

Sex, estradiol, and spatial memory in a food-caching corvid.

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.

Topography of inputs into the hippocampal formation of a food-caching bird.

The mammalian hippocampal formation (HF) is organized into domains associated with different functions. These differences are driven in part by the pattern of input along the hippocampal long axis, such as visual input to the septal hippocampus and amygdalar input to the temporal hippocampus. HF is also organized along the transverse axis, with different patterns of neural activity in the hippocampus and the entorhinal cortex. In some birds, a similar organization has been observed along both of these axes. However, it is not known what role inputs play in this organization. We used retrograde tracing to map inputs into HF of a food-caching bird, the black-capped chickadee. We first compared two locations along the transverse axis: the hippocampus and the dorsolateral hippocampal area (DL), which is analogous to the entorhinal cortex. We found that pallial regions predominantly targeted DL, while some subcortical regions like the lateral hypothalamus (LHy) preferentially targeted the hippocampus. We then examined the hippocampal long axis and found that almost all inputs were topographic along this direction. For example, the anterior hippocampus was preferentially innervated by thalamic regions, while the posterior hippocampus received more amygdalar input. Some of the topographies we found bear a resemblance to those described in the mammalian brain, revealing a remarkable anatomical similarity of phylogenetically distant animals. More generally, our work establishes the pattern of inputs to HF in chickadees. Some of these patterns may be unique to chickadees, laying the groundwork for studying the anatomical basis of these birds' exceptional hippocampal memory.

Flexible use of memory by food-caching birds.

Animals use memory-guided and memory-independent strategies to make navigational decisions. Disentangling the contribution of these strategies to navigation is critical for understanding how memory influences behavioral output. To address this issue, we studied spatial behaviors of the chickadee, a food-caching bird. Chickadees hide food in concealed, scattered locations and retrieve their caches later in time. We designed an apparatus that allows birds to cache and retrieve food at many sites while navigating in a laboratory arena. This apparatus enabled automated tracking of behavioral variables - including caches, retrievals, and investigations of different sites. We built probabilistic models to fit these behavioral data using a combination of mnemonic and non-mnemonic factors. We found that chickadees use some navigational strategies that are independent of cache memories, including opportunistic foraging and spatial biases. They combine these strategies with spatially precise memories of which sites contain caches and which sites they have previously checked. A single memory of site contents is used in a context-dependent manner: during caching chickadees avoid sites that contain food, while during retrieval they instead preferentially access occupied sites. Our approach is a powerful way to investigate navigational decisions in a natural behavior, including flexible contributions of memory to these decisions.

Humans form new memories about what is happening in their lives every day. These autobiographical memories depend on a part of the brain called the hippocampus. But how these memories are recorded remains unclear. Studying certain birds may help to provide more insight. Black-capped chickadees, for example, are memory specialists. They stash thousands of food items and use their memories to recover these hidden food stores. This behavior also relies on these birds' hippocampus. Studying these animals' behavior in the laboratory may help scientists decode how the birds use their memories and to gain more insight about the brain processes underlying memory. Now, Applegate and Aronov show that chickadees use memory not only to retrieve food but also to decide where to hide it in the first place. In the experiments, chickadees were placed in a specialized enclosure with a grid of holes covered by silicone rubber flaps on the floor. The birds lifted the flaps with their toes or beak to hide a piece of sunflower seed underneath. Applegate and Aronov recorded and analyzed the animals' seed hiding and retrieving behavior with a video camera to determine whether the birds were remembering the sites or happening on them by chance. This revealed that black-capped chickadees use the same memories of where they had hidden food in two different ways. When they were hiding new morsels, the birds remembered where they had stashed food and avoided those flaps. When they were retrieving food, the birds knew exactly which flaps to look under. Future experiments using this special enclosure may help scientists monitor what happens in the chickadees' brains during these activities.

The genetic basis of spatial cognitive variation in a food-caching bird.

Spatial cognition is used by most organisms to navigate their environment. Some species rely particularly heavily on specialized spatial cognition to survive, suggesting that a heritable component of cognition may be under natural selection. This idea remains largely untested outside of humans, perhaps because cognition in general is known to be strongly affected by learning and experience.1-4 We investigated the genetic basis of individual variation in spatial cognition used by non-migratory food-caching birds to recover food stores and survive harsh montane winters. Comparing the genomes of wild, free-living birds ranging from best to worst in their performance on a spatial cognitive task revealed significant associations with genes involved in neuron growth and development and hippocampal function. These results identify candidate genes associated with differences in spatial cognition and provide a critical link connecting individual variation in spatial cognition with natural selection. VIDEO ABSTRACT.

Plasticity of Foraging Strategies Adopted by the Painted Ghost Crab, Ocypode gaudichaudii, in Response to in situ Food Resource Manipulation Experiments.

The feeding strategies of Ocypode gaudichaudii at two sandy beaches, Culebra Beach (CB) and Playa Venao (PV) in Panama, were studied via three experiments. Two separate manipulative in situ experiments were conducted to determine how the densities of food resources and the size of the supplemented food offered to the crabs can affect their diet and food handling behavior. The third experiment, a transplantation study, was also conducted to determine the plasticity of the feeding behavior of the displaced crabs. In the first experiment, freshly-emerged crabs showed different feeding modes when washed-sediment was seeded with different densities of diatoms and rove beetles, which suggests that they are optimal foragers. Crabs hoarded food in the second experiment when food augmentation was performed, in which small and large food pellets were placed around the burrows at the beginning and end of the crabs' feeding cycle. All freshly-emerged crabs from both sites foraged on the small pellets outside their burrows and did not cache food; when pellets were provided at the end of the feeding cycle, crabs from CB fed on some of the small pellets and returned to their burrows with the uneaten pellets left on the surface, whereas crabs at PV picked up all the small food pellets and transferred them into their burrows over several trips before plugging their burrow entrances. Only the crabs from PV carried the large food pellets supplemented at the start and end of the feeding cycle into their burrows. In contrast, the crabs at CB often left behind the partially-eaten pellets on the sand surface, probably due to the increased risk of predation associated with the prolonged handling time of the large food pellets. Excavation of the burrows of the crabs that hoarded food showed that all the pellets were deposited at the bend of the burrows, indicating that they were not consumed immediately. Crabs that fed in droves at PV stopped droving and foraged around their burrows after being transplanted to CB. This is the first documentation of food hoarding in a sandy beach macroinvertebrate at a resource-impoverished habitat. The plasticity of feeding strategies adopted by the painted ghost crab in response to different densities of food resources in the habitat could be an adaptation to the dynamic sandy beach environment.

Digging into the behaviour of an active hunting predator: arctic fox prey caching events revealed by accelerometry.

BACKGROUND: Biologging now allows detailed recording of animal movement, thus informing behavioural ecology in ways unthinkable just a few years ago. In particular, combining GPS and accelerometry allows spatially explicit tracking of various behaviours, including predation events in large terrestrial mammalian predators. Specifically, identification of location clusters resulting from prey handling allows efficient location of killing events. For small predators with short prey handling times, however, identifying predation events through technology remains unresolved. We propose that a promising avenue emerges when specific foraging behaviours generate diagnostic acceleration patterns. One such example is the caching behaviour of the arctic fox (Vulpes lagopus), an active hunting predator strongly relying on food storage when living in proximity to bird colonies. METHODS: We equipped 16 Arctic foxes from Bylot Island (Nunavut, Canada) with GPS and accelerometers, yielding 23 fox-summers of movement data. Accelerometers recorded tri-axial acceleration at 50 Hz while we obtained a sample of simultaneous video recordings of fox behaviour. Multiple supervised machine learning algorithms were tested to classify accelerometry data into 4 behaviours: motionless, running, walking and digging, the latter being associated with food caching. Finally, we assessed the spatio-temporal concordance of fox digging and greater snow goose (Anser caerulescens antlanticus) nesting, to test the ecological relevance of our behavioural classification in a well-known study system dominated by top-down trophic interactions. RESULTS: The random forest model yielded the best behavioural classification, with accuracies for each behaviour over 96%. Overall, arctic foxes spent 49% of the time motionless, 34% running, 9% walking, and 8% digging. The probability of digging increased with goose nest density and this result held during both goose egg incubation and brooding periods. CONCLUSIONS: Accelerometry combined with GPS allowed us to track across space and time a critical foraging behaviour from a small active hunting predator, informing on spatio-temporal distribution of predation risk in an Arctic vertebrate community. Our study opens new possibilities for assessing the foraging behaviour of terrestrial predators, a key step to disentangle the subtle mechanisms structuring many predator-prey interactions and trophic networks.

Autumn freeze-thaw events carry over to depress late-winter reproductive performance in Canada jays.

Evidence suggests that range-edge populations are highly vulnerable to the impacts of climate change, but few studies have examined the specific mechanisms that are driving observed declines. Species that store perishable food for extended periods of time may be particularly susceptible to environmental change because shifts in climatic conditions could accelerate the natural degradation of their cached food. Here, we use 40 years of breeding data from a marked population of Canada jays (Perisoreus canadensis) located at the southern edge of their range in Algonquin Provincial Park, Ontario, to examine whether climatic conditions prior to breeding carry over to influence reproductive performance. We found that multiple measures of Canada jay reproductive performance (brood size, nest success and nestling condition) in the late winter were negatively correlated with the number of freeze-thaw events the previous autumn. Our results suggest that freeze-thaw events have a significant detrimental impact on the quality and/or quantity of cached food available to Canada jays. Future increases in such events, caused by climate change, could pose a serious threat to Canada jays and other food caching species that store perishable foods for long periods of time.

Natural Selection and Spatial Cognition in Wild Food-Caching Mountain Chickadees.

Understanding how differences in cognition evolve is one of the critical goals in cognitive ecology [1-5]. In food-caching species that rely on memory to recover caches, enhanced spatial cognition has been hypothesized to evolve via natural selection [2, 6-8], but there has been no direct evidence of natural selection acting on spatial memory. Food-caching mountain chickadees living at harsher, higher elevations, with greater reliance on cached food have better spatial learning abilities and larger hippocampi containing more and larger neurons compared to birds from milder, lower elevations [9, 10]. Here, we tested for natural selection on spatial cognition in wild food-caching mountain chickadees at high elevations and documented the following: (1) compared to first-year juveniles, adults showed significantly better performance on two spatial cognitive tasks-spatial learning and memory and a consecutive reversal learning task; (2) cognitive performance in both spatial learning and reversal learning tasks was not significantly different between years in the same chickadees tested in their first year of life and after surviving to their second winter; and (3) cognitive performance in the spatial learning task was significantly better among the first-year juveniles that survived to their second winter compared to the subset of juveniles that did not survive. Taken together, our results provide evidence for natural selection on spatial cognition in a food-caching species living in harsh environments and suggest that natural selection associated with local environmental conditions might be generating intraspecific differences in cognitive abilities. VIDEO ABSTRACT.