Publications by authors named "Vladimir Pravosudov"

51 Publications

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

Proc Biol Sci 2021 Mar 31;288(1947):20203180. Epub 2021 Mar 31.

Department of Biology, University of Nevada Reno, Reno, NV 89557, USA.

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.
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http://dx.doi.org/10.1098/rspb.2020.3180DOI Listing
March 2021

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

Proc Biol Sci 2020 07 15;287(1931):20200895. Epub 2020 Jul 15.

Ecology, Evolution, and Conservation Biology Graduate Program, University of Nevada Reno, Reno, NV 89557, USA.

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.
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http://dx.doi.org/10.1098/rspb.2020.0895DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7423667PMC
July 2020

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

Ecol Lett 2019 Jun 7;22(6):897-903. Epub 2019 Mar 7.

Ecology, Evolution, and Conservation Biology Graduate Program, University of Nevada, Reno, NV, USA.

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.
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http://dx.doi.org/10.1111/ele.13249DOI Listing
June 2019

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

Curr Biol 2019 02 7;29(4):670-676.e3. Epub 2019 Feb 7.

University of Nevada Reno, Department of Biology and Ecology, Evolution, and Conservation Biology Graduate Program, Reno, NV 89557, USA. Electronic address:

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.
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http://dx.doi.org/10.1016/j.cub.2019.01.006DOI Listing
February 2019

Fluctuations in annual climatic extremes are associated with reproductive variation in resident mountain chickadees.

R Soc Open Sci 2018 May 9;5(5):171604. Epub 2018 May 9.

Department of Biology and Ecology, Evolution and Conservation Doctoral Program, University of Nevada, Reno, NV, USA.

Mounting evidence suggests that we are experiencing rapidly accelerating global climate change. Understanding how climate change may affect life is critical to identifying species and populations that are vulnerable. Most current research focuses on investigating how organisms may respond to gradual warming, but another effect of climate change is extreme annual variation in precipitation associated with alternations between drought and unusually heavy precipitation, like that exhibited in the western regions of North America. Understanding climate change effects on animal reproductive behaviour is especially important, because it directly impacts population persistence. Here, we present data on reproduction in nest-box breeding, resident mountain chickadees inhabiting high and low elevations in the Sierra Nevada across 5 years. These 5 years of data represent the full range of climatic variation from the largest drought in five centuries to one of the heaviest snow years on record. There were significant differences in most reproductive characteristics associated with variation in climate. Both climate extremes were negatively associated with reproductive success at high and low elevations, but low-elevation chickadees had worse reproductive success in the largest drought year while high-elevation chickadees had worse reproductive success in the heaviest snow year. Considering that the frequency of extreme climate swings between drought and snow is predicted to increase, such swings may have negative effects on chickadee populations across the entire elevation gradient, as climatic extremes should favour different adaptations. Alternatively, it is possible that climate fluctuations might favour preserving genetic variation allowing for higher resilience. It is too early to make specific predictions regarding how increased frequency of extreme climate fluctuation may impact chickadees; however, our data suggest that even the most common species may be susceptible.
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http://dx.doi.org/10.1098/rsos.171604DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5990810PMC
May 2018

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

Proc Biol Sci 2017 May;284(1855)

Department of Biology, Evolution and Conservation Biology Doctoral Program, University of Nevada, Reno, NV, USA.

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.
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http://dx.doi.org/10.1098/rspb.2016.2613DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5454252PMC
May 2017

Absence of population structure across elevational gradients despite large phenotypic variation in mountain chickadees ().

R Soc Open Sci 2017 Mar 15;4(3):170057. Epub 2017 Mar 15.

Department of Biology and Graduate Program in Ecology, Evolution, and Conservation Biology , University of Nevada, Reno , Max Fleischmann Agriculture Building, 1664 N. Virginia Street, Reno, NV 89557 , USA.

Montane habitats are characterized by predictably rapid heterogeneity along elevational gradients and are useful for investigating the consequences of environmental heterogeneity for local adaptation and population genetic structure. Food-caching mountain chickadees inhabit a continuous elevation gradient in the Sierra Nevada, and birds living at harsher, high elevations have better spatial memory ability and exhibit differences in male song structure and female mate preference compared to birds inhabiting milder, low elevations. While high elevation birds breed, on average, two weeks later than low elevation birds, the extent of gene flow between elevations is unknown. Despite phenotypic variation and indirect evidence for local adaptation, population genetic analyses based on 18 073 single nucleotide polymorphisms across three transects of high and low elevation populations provided no evidence for genetic differentiation. Analyses based on individual genotypes revealed no patterns of clustering, pairwise estimates of genetic differentiation (, Nei's D) were very low, and AMOVA revealed no evidence for genetic variation structured by transect or by low and high elevation sites within transects. In addition, we found no consistent evidence for strong parallel allele frequency divergence between low and high elevation sites within the three transects. Large elevation-related phenotypic variation may be maintained by strong selection despite gene flow and future work should focus on the mechanisms underlying such variation.
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http://dx.doi.org/10.1098/rsos.170057DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383859PMC
March 2017

Increased Testosterone Decreases Medial Cortical Volume and Neurogenesis in Territorial Side-Blotched Lizards ().

Front Neurosci 2017 1;11:97. Epub 2017 Mar 1.

Department of Biology, University of Nevada Reno, NV, USA.

Variation in an animal's spatial environment can induce variation in the hippocampus, an area of the brain involved in spatial cognitive processing. Specifically, increased spatial area use is correlated with increased hippocampal attributes, such as volume and neurogenesis. In the side-blotched lizard (), males demonstrate alternative reproductive tactics and are either territorial-defending large, clearly defined spatial boundaries-or non-territorial-traversing home ranges that are smaller than the territorial males' territories. Our previous work demonstrated cortical volume (reptilian hippocampal homolog) correlates with these spatial niches. We found that territorial holders have larger medial cortices than non-territory holders, yet these differences in the neural architecture demonstrated some degree of plasticity as well. Although we have demonstrated a link among territoriality, spatial use, and brain plasticity, the mechanisms that underlie this relationship are unclear. Previous studies found that higher testosterone levels can induce increased use of the spatial area and can cause an upregulation in hippocampal attributes. Thus, testosterone may be the mechanistic link between spatial area use and the brain. What remains unclear, however, is if testosterone can affect the cortices independent of spatial experiences and whether testosterone differentially interacts with territorial status to produce the resultant cortical phenotype. In this study, we compared neurogenesis as measured by the total number of doublecortin-positive cells and cortical volume between territorial and non-territorial males supplemented with testosterone. We found no significant differences in the number of doublecortin-positive cells or cortical volume among control territorial, control non-territorial, and testosterone-supplemented non-territorial males, while testosterone-supplemented territorial males had smaller medial cortices containing fewer doublecortin-positive cells. These results demonstrate that testosterone can modulate medial cortical attributes outside of differential spatial processing experiences but that territorial males appear to be more sensitive to alterations in testosterone levels compared with non-territorial males.
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http://dx.doi.org/10.3389/fnins.2017.00097DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5331184PMC
March 2017

Mountain chickadees from different elevations sing different songs: acoustic adaptation, temporal drift or signal of local adaptation?

R Soc Open Sci 2015 Apr 29;2(4):150019. Epub 2015 Apr 29.

Department of Biology and Graduate Program in Ecology, Evolution, and Conservation Biology , University of Nevada , Reno Max Fleischmann Agriculture Building, 1664 North Virginia Street, Reno, NV 89557, USA.

Song in songbirds is widely thought to function in mate choice and male-male competition. Song is also phenotypically plastic and typically learned from local adults; therefore, it varies across geographical space and can serve as a cue for an individual's location of origin, with females commonly preferring males from their respective location. Geographical variation in song dialect may reflect acoustic adaptation to different environments and/or serve as a signal of local adaptation. In montane environments, environmental differences can occur over an elevation gradient, favouring local adaptations across small spatial scales. We tested whether food caching mountain chickadees, known to exhibit elevation-related differences in food caching intensity, spatial memory and the hippocampus, also sing different dialects despite continuous distribution and close proximity. Male songs were collected from high and low elevations at two different mountains (separated by 35 km) to test whether song differs between elevations and/or between adjacent populations at each mountain. Song structure varied significantly between high and low elevation adjacent populations from the same mountain and between populations from different mountains at the same elevations, despite a continuous distribution across each mountain slope. These results suggest that elevation-related differences in song structure in chickadees might serve as a signal for local adaptation.
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http://dx.doi.org/10.1098/rsos.150019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4448878PMC
April 2015

Potential Mechanisms Driving Population Variation in Spatial Memory and the Hippocampus in Food-caching Chickadees.

Integr Comp Biol 2015 Sep 11;55(3):354-71. Epub 2015 May 11.

*Department of Biology, Program in Ecology, Evolution, and Conservation Biology, University of Nevada-Reno, Reno, NV 89557, USA;

Harsh environments and severe winters have been hypothesized to favor improvement of the cognitive abilities necessary for successful foraging. Geographic variation in winter climate, then, is likely associated with differences in selection pressures on cognitive ability, which could lead to evolutionary changes in cognition and its neural mechanisms, assuming that variation in these traits is heritable. Here, we focus on two species of food-caching chickadees (genus Poecile), which rely on stored food for survival over winter and require the use of spatial memory to recover their stores. These species also exhibit extensive climate-related population level variation in spatial memory and the hippocampus, including volume, the total number and size of neurons, and adults' rates of neurogenesis. Such variation could be driven by several mechanisms within the context of natural selection, including independent, population-specific selection (local adaptation), environment experience-based plasticity, developmental differences, and/or epigenetic differences. Extensive data on cognition, brain morphology, and behavior in multiple populations of these two species of chickadees along longitudinal, latitudinal, and elevational gradients in winter climate are most consistent with the hypothesis that natural selection drives the evolution of local adaptations associated with spatial memory differences among populations. Conversely, there is little support for the hypotheses that environment-induced plasticity or developmental differences are the main causes of population differences across climatic gradients. Available data on epigenetic modifications of memory ability are also inconsistent with the observed patterns of population variation, with birds living in more stressful and harsher environments having better spatial memory associated with a larger hippocampus and a larger number of hippocampal neurons. Overall, the existing data are most consistent with the hypothesis that highly predictable differences in winter climate drive the evolution and maintenance of differences among populations both in cognition and in the brain via local adaptations, at least in food-caching parids.
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http://dx.doi.org/10.1093/icb/icv029DOI Listing
September 2015

Chickadees with bigger brains have smaller digestive tracts: a multipopulation comparison.

Brain Behav Evol 2014 24;84(3):172-80. Epub 2014 Jul 24.

Department of Biology, University of Nevada, Reno, Nev., USA.

The factors leading to the evolution of large brain size remain controversial. Brains are metabolically expensive and larger brains demand higher maintenance costs. The expensive-tissue hypothesis suggests that when selection favors larger brains, evolutionary changes in brain size can occur without an overall increase in energetic costs when brain size represents a trade-off with the size of other expensive tissues, such as the digestive tract. Still, support for this hypothesis is equivocal. We compared mean brain mass, digestive tract mass (stomach and gut) and heart mass in 9 populations of black-capped chickadees along a gradient of winter climate severity. Mean brain mass and telencephalon volume showed significant population variation with larger brains associated with harsher winter conditions. Mean population brain mass and telencephalon volume were also negatively related to both stomach and gut mass. Mean population heart mass, on the other hand, was not significantly associated with either mean brain mass or winter climate severity. Mean brain mass was negatively associated with body mass, with chickadees from harsher environments being smaller but having larger brains and smaller digestive tracts. Our results are consistent with the expensive-tissue hypothesis, and suggest that a harsher winter climate might favor larger brains, which might be associated with a reduction in size of the digestive tract. These findings could potentially be a result of population differences in the winter climate diet related to the perishability of more efficient invertebrate-based food caches.
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http://dx.doi.org/10.1159/000363686DOI Listing
June 2015

Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards.

Behav Neurosci 2013 Aug 3;127(4):555-65. Epub 2013 Jun 3.

Department of Biology, University of Nevada, Reno, MS 314, 1664 North Virginia Street, Reno, NV 89557, USA.

Differences in an animal's spatial environment can have dramatic effects on the hippocampus, an area of the brain involved with spatial processing. Animals in spatially impoverished environments have decreased hippocampal attributes. However, we do not know if differences in the spatial environment differentially interact with territorial status, which also covaries with hippocampal attributes. Here, we asked whether territoriality and differential spatial-area use interact to generate different effects on cortical attributes (reptilian hippocampal homologue) in lizards. We compared medial and dorsal cortical attributes between territorial and nonterritorial morphotypes of side-blotched lizards, Uta stansburiana, in larger versus smaller (i.e., spatially impoverished) enclosures. We found that territorial males had increased neurogenesis rates in their medial cortices in larger enclosures when compared with their siblings in smaller enclosures; nonterritorial males had low levels of neurogenesis regardless of enclosure size. Enclosure size had no significant effect on cortical volumes or the total number of neurons in either cortical region. These results suggest that territorial morphotypes may be more sensitive to changes in the spatial environment, thus leading to increases in regulation of neurogenesis in the face of increased spatial processing and physical activity demands.
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http://dx.doi.org/10.1037/a0032852DOI Listing
August 2013

Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution.

Trends Ecol Evol 2013 May 18;28(5):290-6. Epub 2013 Mar 18.

School of Life and Environmental Sciences, Deakin University, Geelong, VIC 3216, Australia.

Across taxa, both neural growth and cognitive function show considerable developmental plasticity. Data from studies of decision making, learning, and discrimination demonstrate that early life conditions have an impact on subsequent neural growth, maintenance, and cognition, with important ecological and evolutionary implications. Here, we provide a synthesis of the evidence that spatial and vocal learning are condition dependent, addressing what is known about their physiological control and the functional explanations. Neural investment is predicted to be affected by environmental conditions, but the shape of the response should depend on the fitness benefits of the cognitive traits under control. From an evolutionary perspective, traits promoting resistance to environmental perturbations should be favored when the cognitive trait is a crucial determinant of fitness.
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http://dx.doi.org/10.1016/j.tree.2013.02.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3640828PMC
May 2013

Variation in hippocampal glial cell numbers in food-caching birds from different climates.

Dev Neurobiol 2013 Jun 20;73(6):480-5. Epub 2013 Mar 20.

Department of Psychology, Franklin and Marshall College, Lancaster, Pennsylvania 17604, USA.

Enhancements to memory are associated with enhanced neural structures that support those capabilities. A great deal of work has examined this relationship in the context of natural variation in spatial memory capability and hippocampal (Hp) structure. Most studies have focused on volumetric and neuron measures, but have seldom examined the role of glial cells. Once considered involved only in supportive functions associated with neurons, the importance of glial cells in cognitive processes, including memory, is gaining more attention. Building upon our previous study on the relationship between the brain, memory, and environmental severity in food-caching birds, we compared the total number of Hp glial cells in wild-sampled and in lab-reared (common garden) black-capped chickadees (Poecile atricapillus) originating from two different environmental extremes. We found that birds from more harsh climate tended to have significantly more Hp glial cells than those from more mild climate and that lab-reared chickadees had significantly fewer Hp glial cells compared to the wild-sampled birds. These results suggest that population differences in glial numbers may be controlled, at least in part, by heritable mechanisms, but glial numbers appear to be additionally regulated by an individual's environment. The pattern of Hp glial cell abundance among our treatment groups closely followed that of the Hp volume, suggesting that Hp glial cell number may be associated with the Hp volume. Unlike Hp neurons, however, the number of Hp glial cells may be, at least in part, affected by an individual's experiences and environment.
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http://dx.doi.org/10.1002/dneu.22074DOI Listing
June 2013

Variation in brain regions associated with fear and learning in contrasting climates.

Brain Behav Evol 2012 26;79(3):181-90. Epub 2012 Jan 26.

Department of Biology, University of Nevada, Reno, Nev., USA.

In environments where resources are difficult to obtain and enhanced cognitive capabilities might be adaptive, brain structures associated with cognitive traits may also be enhanced. In our previous studies, we documented a clear and significant relationship among environmental conditions, memory and hippocampal structure using ten populations of black-capped chickadees (Poecile atricapillus) over a large geographic range. In addition, focusing on just the two populations from the geographical extremes of our large-scale comparison, Alaska and Kansas, we found enhanced problem-solving capabilities and reduced neophobia in a captive-raised population of black-capped chickadees originating from the energetically demanding environment (Alaska) relative to conspecifics from the milder environment (Kansas). Here, we focused on three brain regions, the arcopallium (AP), the nucleus taeniae of the amygdala and the lateral striatum (LSt), that have been implicated to some extent in aspects of these behaviors in order to investigate whether potential differences in these brain areas may be associated with our previously detected differences in cognition. We compared the variation in neuron number and volumes of these regions between these populations, in both wild-caught birds and captive-raised individuals. Consistent with our behavioral observations, wild-caught birds from Kansas had a larger AP volume than their wild-caught conspecifics from Alaska, which possessed a higher density of neurons in the LSt. However, there were no other significant differences between populations in the wild-caught and captive-raised groups. Interestingly, individuals from the wild had larger LSt and AP volumes with more neurons than those raised in captivity. Overall, we provide some evidence that population-related differences in problem solving and neophobia may be associated with differences in volume and neuron numbers of our target brain regions. However, the relationship is not completely clear, and our study raises numerous questions about the relationship between the brain and behavior, especially in captive animals.
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http://dx.doi.org/10.1159/000335421DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3343761PMC
August 2012

Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches.

Eur J Neurosci 2011 Sep;34(6):884-907

Department of Natural and Life Sciences, The Open University of Israel, PO Box 808, Ra'anana 43107, Israel.

During the last few decades, evidence has demonstrated that adult neurogenesis is a well-preserved feature throughout the animal kingdom. In birds, ongoing neuronal addition occurs rather broadly, to a number of brain regions. This review describes adult avian neurogenesis and neuronal recruitment, discusses factors that regulate these processes, and touches upon the question of their genetic control. Several attributes make birds an extremely advantageous model to study neurogenesis. First, song learning exhibits seasonal variation that is associated with seasonal variation in neuronal turnover in some song control brain nuclei, which seems to be regulated via adult neurogenesis. Second, food-caching birds naturally use memory-dependent behavior in learning the locations of thousands of food caches scattered over their home ranges. In comparison with other birds, food-caching species have relatively enlarged hippocampi with more neurons and intense neurogenesis, which appears to be related to spatial learning. Finally, migratory behavior and naturally occurring social systems in birds also provide opportunities to investigate neurogenesis. This diversity of naturally occurring memory-based behaviors, combined with the fact that birds can be studied both in the wild and in the laboratory, make them ideal for investigation of neural processes underlying learning. This can be done by using various approaches, from evolutionary and comparative to neuroethological and molecular. Finally, we connect the avian arena to a broader view by providing a brief comparative and evolutionary overview of adult neurogenesis and by discussing the possible functional role of the new neurons. We conclude by indicating future directions and possible medical applications.
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http://dx.doi.org/10.1111/j.1460-9568.2011.07851.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3177424PMC
September 2011

Evidence for long-term spatial memory in a parid.

Anim Cogn 2012 Mar 20;15(2):149-54. Epub 2011 Jul 20.

Department of Biology, University of Nevada, Reno, NV 89557, USA.

Many animals use spatial memory. Although much work has examined the accuracy of spatial memory, few studies have explicitly focused on its longevity. The importance of long-term spatial memory for foraging has been demonstrated in several cases. However, the importance of such long-term memory for all animals is unclear. In this study, we present the first evidence that a parid species (the black-capped chickadee, Poecile atricapillus) can remember the location of a single food item for at least 6 months under an associative-learning spatial memory paradigm with multiple reinforcements. We did not detect a significant difference in memory longevity between two populations of chickadees shown previously to differ in short-term spatial memory and hippocampal morphology, an area of the brain involved in spatial memory. Our study showed that small birds such as parids can maintain spatial memories for long periods, a feat shown previously only in corvids. Moreover, we were able to demonstrate this longevity within the context of only 16 repeated trials. We speculate that this ability may potentially be useful in relocating caches if reinforced by repeated visits. Future studies are necessary to test whether our results were specifically due to multiple reinforcements of the food-containing location and whether parids may have similar memory longevity during food-caching experiences in the wild.
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http://dx.doi.org/10.1007/s10071-011-0440-3DOI Listing
March 2012

Variation in memory and the hippocampus across populations from different climates: a common garden approach.

Proc Biol Sci 2012 Jan 29;279(1727):402-10. Epub 2011 Jun 29.

Department of Biology, University of Nevada, Reno, NV 89557, USA.

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individual's experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captive-raised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.
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http://dx.doi.org/10.1098/rspb.2011.1020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3223688PMC
January 2012

Variation in hippocampal morphology along an environmental gradient: controlling for the effects of day length.

Proc Biol Sci 2011 Sep 2;278(1718):2662-7. Epub 2011 Feb 2.

Department of Biology, University of Nevada, 1664 North Virginia Street, MS 314, Reno, NV 89557, USA.

Environmental conditions may create increased demands for memory, which in turn may affect specific brain regions responsible for memory function. This may occur either via phenotypic plasticity or selection for individuals with enhanced cognitive abilities. For food-caching animals, in particular, spatial memory appears to be important because it may have a direct effect on fitness via their ability to accurately retrieve food caches. Our previous studies have shown that caching animals living in more harsh environments (characterized by low temperatures, high snow cover and short day lengths) possess more neurons within a larger hippocampus (Hp), a part of the brain involved in spatial memory. However, the relative role of each of these environmental features in the relationship is unknown. Here, we dissociate the effects of one theoretically important factor (day length) within the environmental severity/Hp relationship by examining food-caching birds (black-capped chickadee, Poecile atricapillus) selected at locations along the same latitude, but with very different climatic regimes. There was a significant difference in Hp attributes among populations along the same latitude with very different climatic features. Birds from the climatically mild location had significantly smaller Hp volumes and fewer Hp neurons than birds from the more harsh populations, even though all populations experienced similar day lengths. These results suggest that variables such as temperature and snow cover seem to be important even without the compounding effect of reduced day length at higher latitudes and suggest that low temperature and snow cover alone may be sufficient to generate high demands for memory and the hippocampus. Our data further confirmed that the association between harsh environment and the hippocampus in food-caching animals is robust across a large geographical area and across years.
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http://dx.doi.org/10.1098/rspb.2010.2585DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3136832PMC
September 2011

Hippocampal memory consolidation during sleep: a comparison of mammals and birds.

Biol Rev Camb Philos Soc 2011 Aug 11;86(3):658-91. Epub 2010 Nov 11.

Max Planck Institute for Ornithology, Sleep and Flight Group, Eberhard-Gwinner-Strasse, 82319, Seewiesen, Germany.

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow-wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow-oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high-order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow-oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp-wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7-14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow-oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow-oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region--the caudolateral nidopallium (NCL)--involved in performing high-order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra-hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow-oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow-oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.
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http://dx.doi.org/10.1111/j.1469-185X.2010.00165.xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3117012PMC
August 2011

The effect of environmental harshness on neurogenesis: a large-scale comparison.

Dev Neurobiol 2011 Mar;71(3):246-52

Department of Biology, University of Nevada, Reno, Nevada 89557, USA.

Harsh environmental conditions may produce strong selection pressure on traits, such as memory, that may enhance fitness. Enhanced memory may be crucial for survival in animals that use memory to find food and, thus, particularly important in environments where food sources may be unpredictable. For example, animals that cache and later retrieve their food may exhibit enhanced spatial memory in harsh environments compared with those in mild environments. One way that selection may enhance memory is via the hippocampus, a brain region involved in spatial memory. In a previous study, we established a positive relationship between environmental severity and hippocampal morphology in food-caching black-capped chickadees (Poecile atricapillus). Here, we expanded upon this previous work to investigate the relationship between environmental harshness and neurogenesis, a process that may support hippocampal cytoarchitecture. We report a significant and positive relationship between the degree of environmental harshness across several populations over a large geographic area and (1) the total number of immature hippocampal neurons, (2) the number of immature neurons relative to the hippocampal volume, and (3) the number of immature neurons relative to the total number of hippocampal neurons. Our results suggest that hippocampal neurogenesis may play an important role in environments where increased reliance on memory for cache recovery is critical.
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http://dx.doi.org/10.1002/dneu.20847DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3092529PMC
March 2011

Hippocampal neurogenesis is associated with migratory behaviour in adult but not juvenile sparrows (Zonotrichia leucophrys ssp.).

Proc Biol Sci 2011 Jan 21;278(1702):138-43. Epub 2010 Jul 21.

Department of Biology, University of Nevada, Reno, , 1664 North Virginia Street, MS 314, Reno, NV 89557, USA.

It has been hypothesized that individuals who have higher demands for spatially based behaviours should show increases in hippocampal attributes. Some avian species have been shown to use a spatially based representation of their environment during migration. Further, differences in hippocampal attributes have been shown between migratory and non-migratory subspecies as well as between individuals with and without migratory experience (juveniles versus adults). We tested whether migratory behaviour might also be associated with increased hippocampal neurogenesis, and whether potential differences track previously reported differences in hippocampal attributes between a migratory (Zonotrichia leucophrys gambelii) and non-migratory subspecies (Z. l. nuttalli) of white-crowned sparrows. We found that non-migratory adults had relatively fewer numbers of immature hippocampal neurons than adult migratory birds, while adult non-migrants had a lower density of new hippocampal neurons than adult and juvenile migratory birds and juvenile non-migratory birds. Our results suggest that neurogenesis decreases with age, as juveniles, regardless of migratory status, exhibit similar and higher levels of neurogenesis than non-migratory adults. However, our results also suggest that adult migrants may either seasonally increase or maintain neurogenesis levels comparable to those found in juveniles. Our results thus suggest that migratory behaviour in adults is associated with maintained or increased neurogenesis and the differential production of new neurons may be the mechanism underpinning changes in the hippocampal architecture between adult migratory and non-migratory birds.
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http://dx.doi.org/10.1098/rspb.2010.0861DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2992717PMC
January 2011

Chickadees are selfish group members when it comes to food caching.

Anim Behav 2010 Aug;80(2):175-180

Department of Biology, University of Nevada Reno.

Many food-caching animals live in groups and cache pilferage may be one of the negative consequences of social living. Several hypotheses have been proposed to suggest that individuals may benefit from caching even when cache pilferage is high if all individuals can cache and pilfer equally. Stable groups may hypothetically support the evolution of such "reciprocal pilfering" because all group members may potentially have numerous opportunities to pilfer each other's caches. If that were the case, then we would expect animals cache openly in front of their group members, but to avoid caching in direct view of unknown conspecifics. We tested this hypothesis by allowing mountain chickadees (Poecile gambeli) to cache food in three experimental conditions: (1) with a familiar observer from the same group and with an unfamiliar conspecific observer present; (2) with a familiar observer from the same group only, and (3) without any observers. When presented with both a familiar and an unfamiliar observer, the caching chickadees treated both observers equally by choosing caching sites that were both farther away and out of sight of both observers. When only the familiar observer was present, chickadees shifted their choice of caching sites to the surfaces both away from and out of sight of the observer. When no observers were present, all available caching sites were used equally. Our results thus do not support the reciprocal cache sharing hypothesis and suggest that chickadees try to minimize cache pilferage from both familiar group members and unfamiliar conspecifics.
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http://dx.doi.org/10.1016/j.anbehav.2010.04.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2907166PMC
August 2010

Learning capabilities enhanced in harsh environments: a common garden approach.

Proc Biol Sci 2010 Oct 2;277(1697):3187-93. Epub 2010 Jun 2.

Department of Biology, University of Nevada, MS 314, Reno, NV 89557, USA.

Previous studies have suggested that the ability to inhabit harsh environments may be linked to advanced learning traits. However, it is not clear if individuals express such traits as a consequence of experiencing challenging environments or if these traits are inherited. To assess the influence of differential selection pressures on variation in aspects of cognition, we used a common garden approach to examine the response to novelty and problem-solving abilities of two populations of black-capped chickadees (Poecile atricapillus). These populations originated from the latitudinal extremes of the species's range, where we had previously demonstrated significant differences in memory and brain morphology in a multi-population study. We found that birds from the harsh northern population, where selection for cognitive abilities is expected to be high, significantly outperformed conspecifics from the mild southern population. Our results imply differences in cognitive abilities that may be inherited, as individuals from both populations were raised in and had experienced identical environmental conditions from 10 days of age. Although our data suggest an effect independent of experience, we cannot rule out maternal effects or experiences within the nest prior to day 10 with our design. Nevertheless, our results support the idea that environmental severity may be an important factor in shaping certain aspects of cognition.
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http://dx.doi.org/10.1098/rspb.2010.0630DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982060PMC
October 2010

No effect of social group composition or size on hippocampal formation morphology and neurogenesis in mountain chickadees (Poecile gambeli).

Dev Neurobiol 2010 Jun;70(7):538-47

Department of Biology, University of Nevada, Reno, Nevada, USA.

Brain plasticity and adult neurogenesis may play a role in many ecologically important processes including mate recognition, song learning and production, and spatial memory processing. In a number of species, both physical and social environments appear to influence attributes (e.g., volume, neuron number, and neurogenesis) of particular brain regions. The hippocampus in particular is well known to be especially sensitive to such changes. Although social grouping in many taxa includes the formation of male and female pairs, most studies of the relationship between social environment and the hippocampus have typically considered only solitary animals and those living in same-sex groups. Thus, the aim of this study was to compare the volume of the hippocampal formation, the total number of hippocampal neurons, and the number of immature neurons in the hippocampus (as determined by doublecortin expression) in mountain chickadees (Poecile gambeli) housed in groups of males and females, male-female pairs, same sex pairs of either males or females, and as solitary individuals. The different groups were visually and physically, but not acoustically, isolated from each other. We found no significant differences between any of our groups in hippocampal volume, the total number of hippocampal neurons, or the number of immature neurons. Our results thus provided no support to the hypothesis that social group composition and/or size have an effect on hippocampal morphology and neurogenesis.
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http://dx.doi.org/10.1002/dneu.20795DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2913135PMC
June 2010

Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies.

Anim Behav 2009 Jul;78(1):91-96

University of Nevada, Reno Biology Department.

Spatial abilities have been associated with many ecologically-relevant behaviors such as territoriality, mate choice, navigation and acquisition of food resources. Differential demands on spatial abilities in birds and mammals have been shown to affect the hippocampus, the region of the brain responsible for spatial processing. In some bird and mammal species, higher demands on spatial abilities are associated with larger hippocampal volumes. The medial and dorsal cortices are the putative reptilian homologues of the mammalian hippocampus, yet few studies have examined the relationship between these brain areas and differential spatial use strategies in reptiles. Further, many studies in birds and mammals compare hippocampal attributes between species that utilize space differently, potentially confounding species-specific effects with effects due to differential behaviors in spatial use. Here, we investigated the relationship between spatial use strategies and medial and dorsal cortical volumes in males of the side-blotched lizard (Uta stansburiana). In this species, males occur in three different morphs, each morph using different spatial niches: large territory holders, small territory holders and non-territory holders with home ranges smaller than the territories of small territory holders. We found that large territory holders had larger dorsal cortical volumes relative to the remainder of the telencephalon compared with non-territorial males, and small territory holders were intermediate. These results suggest that some aspect of holding a large territory may place demands on spatial abilities, which is reflected in a brain region thought partially responsible for spatial processing.
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http://dx.doi.org/10.1016/j.anbehav.2009.03.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2701711PMC
July 2009

Behavioral Profile Predicts Dominance Status in Mountain Chickadees.

Anim Behav 2009 Jun;77(6):1441-1448

Department of Biology, University of Nevada, Reno.

Individual variation in stable behavioral traits may explain variation in ecologically-relevant behaviors such as foraging, dispersal, anti-predator behavior, and dominance. We investigated behavioral variation in mountain chickadees (Poecile gambeli), a North American parid that lives in dominance-structured winter flocks, using two common measures of behavioral profile: exploration of a novel room and novel object exploration. We related those behavioral traits to dominance status in male chickadees following brief, pair-wise encounters. Low-exploring birds (birds that visited less than four locations in the novel room) were significantly more likely to become dominant in brief, pairwise encounters with high-exploring birds (i.e., birds that visited all perching locations within a novel room). On the other hand, there was no relationship between novel object exploration and dominance. Interestingly, novel room exploration was also not correlated with novel object exploration. These results suggest that behavioral profile may predict the social status of group-living individuals. Moreover, our results contradict the idea that novel object exploration and novel room exploration are always interchangeable measures of individuals' sensitivity to environmental novelty.
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http://dx.doi.org/10.1016/j.anbehav.2009.02.022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2712732PMC
June 2009

The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation.

Philos Trans R Soc Lond B Biol Sci 2010 Mar;365(1542):945-59

Department of Biology, University of Nevada, Reno, NV 89557, USA.

All animals in which sleep has been studied express signs of sleep-like behaviour, suggesting that sleep must have some fundamental functions that are sustained by natural selection. Those functions, however, are still not clear. Here, we examine the ecological relevance of sleep from the perspective of behavioural trade-offs that might affect fitness. Specifically, we highlight the advantage of using food-caching animals as a system in which a conflict might occur between engaging in sleep for memory/learning and hypothermia/torpor to conserve energy. We briefly review the evidence for the importance of sleep for memory, the importance of memory for food-caching animals and the conflicts that might occur between sleep and energy conservation in these animals. We suggest that the food-caching paradigm represents a naturalistic and experimentally practical system that provides the opportunity for a new direction in sleep research that will expand our understanding of sleep, especially within the context of ecological and evolutionary processes.
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http://dx.doi.org/10.1098/rstb.2009.0209DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2830243PMC
March 2010

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus.

Philos Trans R Soc Lond B Biol Sci 2010 Mar;365(1542):915-31

Department of Biology, University of Nevada, Reno, NV 89557, USA.

A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.
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http://dx.doi.org/10.1098/rstb.2009.0208DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2830242PMC
March 2010