Vladimir V. Pravosudov - US grants

Food-storing birds rely on their food caches to survive winters and use spatial memory for successful food recovery. Both theoretical and empirical studies suggest that energetically demanding ecological conditions should result in more intensive food caching. Thus, environmental conditions that place higher demands on spatial memory and the hippocampus result in enhanced spatial memory and an enlarged hippocampus with more neurons will be investigated. A comparative method and a common garden experiment will be used to test a prediction that black-capped chickadees in northern populations have evolved enhanced spatial memory and an enlarged hippocampus with more neurons. First, hippocampal structure in black-capped chickadees from twelve populations along a latitudinal gradient will be compared. Theoretical models also suggest that more caching along with successful cache recovery should significantly increase the probability of survival in birds specifically when environmental conditions are more energetically demanding and unpredictable like those in northern locations. Therefore chickadees living in more northern environments should depend on caches more heavily because of harsher winter conditions, and thus should experience higher demands for spatial memory than their more southern conspecifics. To determine whether differences in memory and the hippocampus between northern and southern chickadees have evolved, a common garden experiment in which northern and southern black-capped chickadees taken from nests and hand-raised under identical laboratory conditions will be conducted to test two predictions from the adaptive specialization hypothesis: (1) individuals in northern populations should have a relatively larger hippocampus with more neurons and higher cell proliferation rates; and (2) these differences between northern and southern populations have evolved as a result of greater selection pressure on memory and the hippocampus and thus they have a genetic basis. Studying the relationship between environment, memory and the hippocampus in birds will advance our understanding of the evolution of memory and the brain. The proposed activity will provide interdisciplinary research training to one postdoctoral associate, to 2-3 undergraduate students and to 1-2 interns from a community college per year. Every effort will be made to recruit candidates for these positions from underrepresented groups in the biological sciences. The results of the study will be presented at national and international meetings, and published in peer-reviewed journals. Results and rationale of the proposed study will made available to a broader audience through a freely accessible web site, publications in popular media, presentations at local community colleges and through teaching undergraduate classes. All processed brain tissue will be used in teaching undergraduate and graduate students. The proposed study is interdisciplinary and it will bolster integration between the fields of behavioral ecology, neurobiology, and endocrinology.

[unreadable] DESCRIPTION (provided by applicant): Environmental conditions could be critical for maintaining mental health including memory and its neural mechanisms. Whereas much attention has been devoted to the effects of enriched physical environment on memory and the hippocampus, the effects of social environment remain poorly investigated. Many animal species including humans are highly social and complex social interactions are an integral part of their natural environment. To understand maintenance of healthy memory and neurological consequences of social disorders, it is it crucial to investigate how social environment might influence memory and the brain. The proposed study will investigate the relationship between social environment, memory, hippocampal structure and neurogenesis using a food-caching bird, mountain chickadee, as a model. Hippocampus, which is involved in memory function, is well known for its plasticity and there is growing evidence that new neurons are generated in the hippocampus throughout adult life span. The proposed study will specifically investigate whether naturally rich social environment is required for maintaining healthy memory and the brain and whether social isolation results in impaired memory, fewer hippocampal neurons and reduced neurogenesis rates including both cell proliferation and neuron survival. Fully grown birds of the same age will be randomly assigned to five different social environments: solitary, unisex male pairs, unisex female pairs, male-female pairs and groups including two male-female pairs. Adult humans and chickadees naturally exist in large groups consisting of male-female pairs - thus the last experimental group will represent the most natural social environment. All birds will be maintained in cages providing equal space per bird for all groups. All birds will be maintained in their assigned social environment for 90 days during which they will be regularly tested in various memory tasks. At the end of the experiment all birds will be sacrificed for the analyses of the hippocampus structure (volume, neuron count) and neurogenesis (using BrdU and Phospho-histone H3 Mitosis markers). This study will provide important information on the effects of social environment on memory and the hippocampus which, in turn, might help better understand consequences of social disorders for mental health and the brain. [unreadable] [unreadable] [unreadable]

[unreadable] DESCRIPTION (provided by applicant): There is growing evidence that new neurons are generated in the hippocampus of adult animals throughout life and it has been hypothesized that hippocampal neurogenesis plays a critical role in memory function. Memory is an important component of mental health and thus it is crucial to understand regulation of neurogenesis. The proposed study will investigate the relationship between environmental complexity and hippocampal plasticity in food-caching birds. Enriched environment appears to induce adult neurogenesis but it is not clear which specific aspects of environment are responsible for facilitating neurogenesis. In addition, all experiments investigating environmental enrichment have been done in laboratory conditions, which are always poor compared to natural environment. This study will investigate whether natural memory-based experiences are necessary to maintain hippocampal structure and whether lack of such experiences results in reduced hippocampal volume, loss of hippocampal neurons and reduced neurogenesis using a novel animal model - food-caching birds. Food-caching birds are heavily dependent on memory to find previously made food caches and cache-recovery behavior presents a great natural model to study memory and the brain both in controlled laboratory and natural conditions. Birds living in natural conditions will be compared to the birds maintained in standard and in enriched laboratory conditions to establish whether hippocampal neurogenesis in enriched laboratory conditions is comparable to that in animals living in natural environments. The overall aim of this proposal is to evaluate the relationships between natural memory-based experiences and the hippocampus both in laboratory and in natural conditions using a novel animal model. This study will provide new information on the effects of memory exercise on the hippocampal structure and neurogenesis, which have important implications for memory and mental health. The proposed study will investigate whether exercising memory is necessary for maintaining healthy memory and the hippocampus, an area of the brain involved in memory function and whether diverse environment is needed for brain maintenance. Memory is an important aspect of mental health and the proposed research will provide new insights into better understanding of human memory disorders. [unreadable] [unreadable] [unreadable]

Spatial memory use has been associated with many behaviors such as territoriality, mate choice, navigation and acquisition of food resources. Differential demands on spatial abilities have been shown to affect the hippocampus, the region of the brain thought partially responsible for spatial processing. Although many studies have found a positive association between space use strategies and hippocampal structure, little is known about the causes of variation in the hippocampus and if or how genetics, experience, hormonal and maternal effects influence this variation. More importantly, while most studies assume fitness consequences based on hippocampal variation, there have been no tests of this assumption. The primary goal of this research is to look at the genetic, maternal, hormonal, and experiential basis of variation in the volume, number of neurons and neurogenesis in the hippocampus, as well as the fitness consequences of variation in the hippocampus of male side-blotched lizards (Uta stansburiana). Consequently, this study has 5 primary goals: (1) to determine whether changes in the hippocampus are genetically encoded and relate to particular genetic combinations, (2) to explore if maternal effects, in the form of estradiol deposition in egg yolk, can cause variation in the hippocampus, (3) to manipulate testosterone in males to gauge if differences in gonadal hormones mediate underlying changes in hippocampal morphology, (4) to explore if changes in the hippocampus can be induced or enhanced by spatial use experiences, and (5) to assess if natural and lesion-induced variation in hippocampal attributes relate to fitness, namely survival. Thus, this research links the mechanism, developmental and fitness consequences of variation in the hippocampus. This study will provide interdisciplinary research training to underrepresented undergraduate students, as well as educating the general public via K-12 scientific videogames, popular print, visual media and presentations at community colleges.

There are large differences in cognitive abilities and brain morphology both within and between species, yet it remains unclear why such differences exist. Such differences may result from differential biological fitness associated with individual variation in cognitive abilities, yet empirical evidence for this hypothesis is lacking. Different tasks require different cognitive abilities (e.g. spatial memory vs. memory for color), yet whether natural selection can shape different cognitive abilities independently is also debated.

The proposed research will address these two major questions by (1) comparing individual differences in two cognitive abilities (spatial learning and non-spatial learning in wild food-caching mountain chickadees in two environments that place different demands on just one of these abilities, spatial memory, which is involved in recovering thousands of previously made food caches and (2) measuring biological fitness associated with individual differences in both cognitive abilities. If natural selection can affect these abilities independently, only differences in spatial learning ability should be associated with differential biological fitness.

In addition to addressing major evolutionary questions about population/species differences in cognitive abilities, the proposed study will also have significant implications for learning and memory research. It is still generally assumed that the mechanisms underlying associative learning in general are the same for all types of learning and memory and so studying one type of memory allows development of treatments for all memory types. Demonstrating that natural selection can affect different cognitive abilities independently would suggest that we must consider specific cognitive abilities and their regulatory mechanisms individually when designing interventions. The proposed research will also increase research readiness and science literacy by providing intensive research training to undergraduate and graduate students as well as outreach to K-12 students and the general public through the Sagehen Biological Station.

It has long been proposed that female animals use various external information containing signals to assess male quality when choosing mates. However, the connection between a male's level of intelligence and external traits that females can assess has been difficult to measure. Here the researchers will assess spatial memory ability, an intelligence trait thought to increase survival in wild food-storing birds, and two overt male signals, feather coloration and song production, to address the question of whether or not female mating choice is associated with these traits. The researchers will conduct the experiments with free-living birds using arrays of programmable 'smart' bird feeders that can track which individuals are using these feeders to test spatial learning ability. The researchers will then test whether individual variation in learning is associated with variation in communication signals and with mate choice. Findings from this work can be applied to a wide variety of species, including humans, that must make important decisions when using information that isn't always easily assessed or tangible. All of the results and findings will be widely available to a variety of audiences through publication in peer-reviewed journals and participation in professional conferences. Additionally, this work will support the research experience of undergraduate students and the equipment used in this project will also be used in public outreach activities in the community, including creating a museum display at the University of Nevada's Museum of Natural History that illustrates the differences in human and non-human.

Signals are universally used across taxa to convey a diverse range of information, including social status, foraging locations, and predator presence. Several hypotheses have been proposed regarding how sexual signals of quality, in particular, have evolved to be honest as these signals are only useful insofar as they reflect some fitness associated trait(s) of the sender. Cognitive ability is one such fitness-related trait, yet direct evidence linking cognitive ability, signaling, and associated fitness consequences of female mating choices have historically been difficult to assess. Using wild birds fitted with passive integrated transponder leg bands and radio-frequency identification technology, the researchers will directly test whether (a) individual variation in a cognitive ability is associated with variation in two modes of signaling perceivable by females and (b) whether variation in cognitive ability and these two signals reflect female mating choices via production of extra-pair offspring. By doing so, the researchers will connect a cognitive trait thought to increase survival, with song production and plumage reflectance, to female mating choices in wild food-caching birds. These birds inhabit differentially harsh environments creating differential selection pressures on spatial memory ability used to retrieve cached food. Using this system the researchers will be able to directly test the assumption that signals reflect individual quality, an assumption that has been somewhat intangible in the past.

Understanding the evolution of cognition and whether natural selection can shape cognitive abilities, is a major goal of the study of animal behavior and evolutionary biology. Cognition allows animals to adjust to changing conditions, and it is well known to be affected by both environmental and developmental conditions. At the same time, there is considerable variation in cognitive abilities both between and within species and causes of such variation remain unclear. It is generally assumed that variation in cognitive abilities can be shaped directly by natural selection and recently, we provided evidence that individual variation in spatial cognitive abilities involved in the recovery of food caches in food-caching mountain chickadees is under direct selection. Mountain chickadees are small birds that rely on their memory to hide and find thousands of food items and depend on their food caches for overwinter survival. The central goal of the research is to understand how natural selection shapes learning and memory ability and to uncover the genetic basis of variation in learning and memory ability. To share the importance of our research with a broad audience, we will use a multifaceted broader impacts strategy focused on student training, community engagement, and education with an overall focus on broadening participation of underrepresented groups through a commitment to equity, inclusion, and diversity. We will engage the general public through public lectures at two field stations and both general public and students from local schools at Natural History Museums in Nevada and in Colorado. The project will provide training to two postdoctoral fellows as well as to numerous graduate and undergraduate students, who will be recruited through established programs that support students traditionally underrepresented in STEM.

This research has four aims. The first is to understand the genetic basis of specialized spatial memory in food-caching mountain chickadees. The second is to measure heritability of specialized spatial memory. The third is to understand how natural selection shapes genetic variation in genomic regions that underlie specialized spatial memory. The fourth is to determine if the genetic basis of spatial memory is geographically consistent by comparing populations from different mountain ranges. To meet these aims, the research will sample mountain chickadees from populations in two different mountain ranges. Among other data types, the work will combine whole genome sequence data, sequence capture data, and spatial cognition data to develop a deep understanding of the mechanisms by which natural selection shapes variation in spatial cognition. This work is jointly funded by the Behavioral Systems Cluster in the Division of Integrative Organismal Systems and the Evolutionary Processes Cluster in the Division of Environmental Biology.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.