Susan C. Alberts - US grants

Susan C. Alberts and Jeanne Altmann:
Proposal number 0322781(Altmann)/0322613(Alberts), Collaborative Research:
Relationship among demographic, social and genetic structure.

Behavior plays a pivotal role in survival and reproduction. Its immediate, short-term impact is in maintaining homeostasis and organismal integrity as behavior provides the individual with a mechanism of rapid and flexible response to changes in its internal and external environments. Even more profound is behavior's long-term impact on the lives of individuals and on the evolutionary trajectories of populations. The main long-term objective of the investigators is to develop a comprehensive picture of how behavior shapes fitness outcomes and population processes in one population of wild mammals - the savanna baboons of the Amboseli basin in east Africa. The proposed work not only will accomplish important short-term goals but will reach overtly toward the long-term ones as well.

The overall conceptual framework is an integrative socioecology that is sensitive to the intrinsic interdependencies among behavior, physiology, genetic structure, and demography. During the next three years, the research will (1) probe more deeply into the function and lifetime development of relationships through individuals' paternal as well as maternal lineage and (2) continue to delineate sources of lifetime fitness differences for both sexes. This will be accomplished by testing eight explicit predictions derived from three hypotheses. For females, these relate to the impact of social status and of paternal and maternal relatives on fitness. For males they address the relationship between mating success and paternity success, the role of male mate choice in paternity success, and the direct behavioral contributions that males make to the survival of their offspring. Genetic and physiological analyses are based on non-invasive biological sampling and associated assay and genotyping techniques, the development and refinement of which have been a cornerstone of these research groups.

CAREER: Social behavior and genetics in a fission-fusion society. Susan C. Alberts

Focusing on a wild population of African elephants, the proposed project will test critical hypotheses about the evolution of social behavior, using both behavioral data and genetic techniques. These hypotheses address (1) the causes of differences in mating success among males, (2) the extent and mechanisms of inbreeding avoidance, (3) the extent to which social relationships are determined by kinship, and (4) the impact of behavior on the genetic structure of populations. The questions addressed in this proposal are of both general importance for understanding the evolution of social behavior, and of particular importance for understanding the relationship between behavior and genes in a well-studied population of a threatened species.
The work will involve the African elephant population in Amboseli National Park, Kenya, which has been the subject of ongoing behavioral and demographic studies since 1974. Elephants, like many social mammals, exhibit long-term associations among female relatives, and mating behavior that favors a class of socially dominant males. However, unlike most mammals, elephants exhibit a very fluid form of fission-fusion society, in which an individual elephant may associate with almost every member of the population in a given year. This raises unique questions about inbreeding avoidance where relatives encounter each other unpredictably, about cooperation in unstable social settings, and about genetic differentiation and gene flow within and between fluid societies. The genetic component of the project will include a large-scale microsatellite analysis and a study of mitochondrial DNA, focusing on 400 individuals. These genetic data will be used to establish (1) paternity for a subset of calves, (2) levels of relatedness between breeding females and males, (3) levels of genetic relatedness between females in focal families, and (4) the distribution of maternal and paternal kin networks within and across families.
The educational component of the project includes graduate and undergraduate course development, as well as the development of a workshop for Durham area high school biology teachers, who have expressed a pressing need for additional course content for their classrooms. Durham area public schools have a high (>60%) minority enrollment as well as a strong commitment to science education, including the teaching of evolution. The workshop aims to provide course content in behavioral ecology, and to capitalize on the strong popular appeal of this sub-discipline in order to increase interest in basic biological research among Durham's diverse student population.

Environmental change is a cornerstone of major theories of human origins. Adaptation to environmental variability--seasonal, random, and directional over decades--is also a key feature of savanna baboons, a large, widespread species of non-human primates that shares many features with humans. The current investigations will focus on the baboon population of Amboseli, a population that has experienced extensive environmental change over the past several decades for which information is available, and that has persisted in the face of this environmental change. Behavior, the centerpiece of the current investigations, plays a pivotal role in adaptation to environmental variability. It has both immediate, short-term consequences for maintaining internal stability and profound long-term consequences for the lives of individuals and for the evolutionary trajectories of populations

The current project will evaluate and test predictions about behavioral and physiological consequences of environmental change, and about the effects of environmental change on birth and death rates. Estimates of gene flow patterns in the study population will also be developed using newly applied statistical methods in combination with genetic markers. By incorporating demographic, behavioral, environmental, genetic, and hormonal data in an integrative framework, the work will serve several specific goals. (1) It will provide detailed information on how environmental change affects fitness components and related traits. (2) It will elucidate the extent to which individuals are differentially affected by, and respond to, environmental change. This will provide important insight into traits that confer an adaptive advantage in the face of environmental change. (3) It will provide important information on the impact of short time-scale environmental change, and on the population structure of a species experiencing such change. (4) It will provide vital data on how organisms adapt to environmental change. This is highly relevant for biological conservation in the current period of rapid, anthropogenic climate change. This project is, of necessity and design, intrinsically interdisciplinary. It will both utilize and enhance integration of concepts, data, and techniques across a range of social and biological sciences.

This project will greatly expand the investigators' long history of training American and Kenyan students-training activities that are intimately connected with the research goals. Recent human resource development has focused on training for 6 post-doctoral fellows, 7 Ph.D. candidates (2 of them Kenyan), 3 M.Sc. students (2 of them Kenyan), 24 undergraduates (including 5 African-Americans and 3 Hispanic women), and 1 high school student. The investigators also actively collaborate with 4 Kenyan scientists and are working with them on relevant in-country capacity-building activities. Proposed exchange visits and a working group meeting in Kenya will further advance these goals and lay an even more solid base for enduring impact.

The project will also extend the investigators' activities toward enhancement of infrastructure and dissemination of results. The PIs are among the first to refine and apply non-invasive techniques for obtaining and utilizing genetic and hormonal samples, techniques that are of increasing importance worldwide for ethical, scientific, and regulatory reasons. In addition, a major task of the investigators in the past few years has been to design and implement a comprehensive database that includes the many diverse data sets associated with the long-term baboon project. The database design has been shared with a number of other scientists upon request. In addition, a website has been developed for their field research project (www.princeton.edu/~baboon), which serves as a vehicle for providing information and data to the public, students from K through post-graduate, and colleagues.

Behavioral responses of male African elephants (Loxodonta africana) to musth urine.

PI: Susan C. Alberts and Julie Hollister-Smith

Male elephants generally exhibit the dominance relationships seen in males of most mammalian societies; a larger individual is dominant to a smaller individual. However, musth episodes (periods of elevated testosterone and high aggression) temporarily raise a male's dominance position above any non-musth male regardless of size or age. Typified by increased association with females, increased sexual activity, temporal gland secretions and nearly continual urine dribbling, musth has been described as similar to rut in ungulates. Unlike rut, however, musth occurs throughout the year and is asynchronous in a population, so that only a few bulls are in musth concurrently. The mechanisms underlying its onset and duration are not well understood, but age, size and physical condition all affect the likelihood that an individual will experience musth. A single musth period may last from just a few days to over five months, generally increasing as a male ages. Maintaining the condition is energetically costly, thus a male physically declines as it continues.
This study explores the potential for chemical signaling between male African elephants via urine dribbling during musth. By examining the temporal patterns of signaling during musth, this study investigates how population level asynchrony of musth may in part be explained by individual economics of maintaining this physiologically expensive condition and of avoiding direct competition with other males in musth. As such, these results may shed additional light on current theories of sexual selection, signaling theory, and male competition strategies. This study also lays the groundwork for future exploration of possible suppression or stimulation of musth in males via urinary signals of musth.

The Robert Noyce Scholarship Program at Duke University provides funding to train eleven secondary science and mathematics teachers per year over a three-year period for a total of 33 students completing the master's degree in teaching. The recruitment of under-represented minorities and undergraduates who might not consider teaching is emphasized. The Program is increasing the number of highly trained mathematics and science teachers who have advanced study in their teaching discipline and extended teaching experience under the direction of highly skilled mentors. By training in the Durham Public Schools, a high-need school system, these teachers are well prepared to begin their careers in similar school systems where the need for qualified mathematics and science teachers is greatest. Students complete five graduate level courses in their teaching field in addition to course work in education. The teaching internship takes place under the direction of a career teacher who has received extensive training in mentoring and adult development. The internship covers one full semester and a portion of the second semester so that all participating students gain extensive experience teaching high school students in a variety of disciplinary courses and at various performance levels. Each teaching intern works with high school students who are not fluent in English and with students who have been identified with special learning needs in addition to high performing students in advanced placement classes.

Understanding the relationship between genes and organism-level traits (phenotypes) is one of the most important problems in biology today. This relationship is especially important to study in primates, the closest living relatives of humans. The goal of this work is to examine this relationship in one well-studied population of wild primates, the baboons of the Amboseli basin in southern Kenya. Using a set of immune system genes, the researchers will (1) describe genetic variation in the regulatory regions of these genes (the regions that determine when and how much these genes are expressed), (2) determine the exact nature of the subset of genetic variation that affects how much these genes are expressed, and (3) connect this gene expression data to long-term behavioral and ecological data on the study population, to see how gene expression is modified by the environment. This represents ground-breaking work, because it is the first study to examine genetic variation and gene expression in a wild primate population, one for which extensive data already exist on organism-level traits and the environment in which they occur.

Intellectual merit. The proposed work has great potential to advance understanding of the relationship between genes, organism-level traits, and the environment. Further, it is one of the first modern molecular population genetic studies to be conducted on wild animals. In addition, it will generate novel data sets on population genetic and gene expression variation in a wild primate.

Broader impacts. This research will support the production of samples and datasets of interest to the larger scientific community and will contribute to the ongoing training of three Kenyan field assistants. In addition, it will foster integrative research in the field through using molecular genetic techniques to address anthropological and evolutionary questions. Finally, it will contribute to the training of a graduate student and undergraduates interested in anthropological research.

Understanding the expression and evolution of complex traits requires, among other things, measuring the genetic variation that underlies these traits. This in turn requires an understanding of the interplay between genes, the environment, and the traits an organism displays, specifically the nature of gene by environment interactions (GEIs). GEIs arise when two different genotypes respond differently to a change in the environment. Surprisingly little is known about GEIs in natural populations, although GEIs are pervasive in all known organisms, including humans. This project will address this gap by examining multiple aspects of GEIs in a wild mammal population. The project takes advantage of a long-term field study of wild baboons in the Amboseli basin in southern Kenya, in which individually known animals have been under continuous observation for 38 years. The investigators will test hypotheses about the ways in which GEIs influence variation in traits of adult baboons, and the manner in which GEIs affect standing genetic variation.

The proposed project will continue and extend the investigators' long history of training American and Kenyan students. The project will generate several unique data sets that will be of interest to the wider scientific community, and which are available for no other natural primate population. In addition, PIs have shared the design and implementation of their comprehensive long term database (BABASE) with a number of other scientists, and have also developed a website for the research project (www.princeton.edu/~baboon) which serves as a vehicle for providing information and data to the public.

DESCRIPTION (provided by applicant): Studies of aging in wild animal populations, especially in our primate relatives, offer a unique set of potential benefits for understanding the processes and patterns governing human aging. The comparative perspective that animal models provide can both bring to light general principles and mechanisms that govern the aging process across species, and can highlight human-specific characteristics of aging. Additionally, in some cases datasets that are extremely difficult to gather in humans (such as fine-scaled behavioral data in natural social settings) are more readily obtainable in wild primate populations. However, despite keen interest in aging as a human health concern and the enormous progress in this area in recent decades, patterns of aging in wild animals - age-related changes not just in survival, but also in social behavior, hormone profiles, and other aspects of health and functioning - remain almost entirely undescribed. Our detailed, longitudinal data from a population of wild baboons in southern Kenya provides clear evidence both that senescence occurs, and that considerable variance among individuals is seen both in lifespan and in functional declines with age. Baboons live in stable social groups, and individuals within groups share common environments, so physical and demographic differences alone cannot account for the observed variance in the aging process and in lifespan. However, the quality and robustness of individual social relationships do vary among individuals, both within and between social groups, and this variation has both physiological and functional consequences for baboons. These results have brought social connectedness to the foreground in our ongoing, integrative analysis of variance in lifetime outcomes in this population, and have set the stage for a detailed investigation of the dynamics of social connectedness and its relationship to aging. The goals of the proposed work are to identify the components, physiological correlates, and consequences of social connectedness in the context of aging, and to identify genetic and environmental sources of variance in social connectedness. We will test the hypotheses that, in wild nonhuman primates as in humans, social connectedness is a predictor of health and well being throughout the life course;that this effect is independent of density;and that social connectedness declines with age. We will then investigate the relationship between genetic variation in a set of known biological pathways and social connectedness phenotypes. Finally, we will integrate the effects of genetic variation and environmental variation into a life span approach, using a time-series model. We will ask whether the effects that occur in earlier stages of life propagate into late life, or if social connectedness in late life is a relatively independent phenomenon. This analysis will aid in identifying stages during the life course in which prediction of and/or intervention in aging- related outcomes may be most fruitful. PUBLIC HEALTH RELEVANCE: The proposed research will investigate health and well being during aging in a natural population of wild primates, which are closely related to humans and share key similarities, but also important differences. The research will specifically examine the contribution of social connectedness to aging-related outcomes in a natural setting, as well as the genetic and environmental contributors to social connectedness itself. This will offer potential benefits for human health by illuminating important opportunities for, and constraints on, alleviating age- related declines in human health and survival.

The long-term objective in this study is to develop a comprehensive picture of how behavior shapes population dynamics and individual life history outcomes in one population of wild mammals, the savanna baboons of the Amboseli basin in east Africa. The overall conceptual framework is concerned with how behavior affects survival and reproduction across the life time, as well as how behavior affects physiology and population genetics. Throughout their long-term work, the investigators have focused on a series of short-term goals that represent components of their long-term objective. With this LTREB project they overtly reach toward one longer-term goal. Specifically, they will follow the ongoing process of genetic admixture (hybridization) between a study population of primarily yellow baboons and neighboring populations of anubis (olive) baboons (a separate subspecies) in order to understand the way in which behavior impacts, and is in turn affected by hybridization. Their previous work has documented rather dramatic differences between hybrid and yellow baboons. This represents a unique opportunity to follow a natural process of population admixture over time, and to test hypotheses about its behavioral causes and consequences. This project is relevant to understanding speciation because of the role that hybridization can play in speciation. It is also relevant to understanding human evolution because of the close ecological parallels between baboons and humans, and the similarity between the baboon radiation in Africa and the evolutionary history of various human species.
The proposed project will continue the investigators' long history of training American and Kenyan students, activities that are intimately connected with the research goals. Recent integration of research and education has focused on training for 13 post-doctoral fellows, 12 doctoral candidates, 5 Master's Degree students, 34 undergraduates, and 2 high school students. The investigators also actively collaborate with Kenyan scientists and are working with them on in-country capacity building.

DESCRIPTION (provided by applicant): Advancing our understanding of social and behavioral effects in aging will increasingly require the integration of complex and often disparate data sets To measure such effects, investigators must manage demographic data on mortality and fertility, behavioral or survey data on social relationships, and, increasingly, biomarker data tha capture genetic and physiological variation. Currently, extant databases are designed to facilitate analysis of complex demographic and sociobehavioral data or complex genetic and genomic data: databases that meet the challenge of integrating all of these data types do not yet exist. Consequently, the research community is not reaping the full benefits of these data sets for understanding aging. Further, we lack models for how to house these data types together in a cohesive and accessible fashion. We propose to develop such a model by building on an existing database on wild primates that houses individual-based multidimensional, longitudinal phenotypic data that have already proved valuable for studies of social and behavioral effects on aging. We also have a growing set of complementary genetic and genomic data on the same individuals, including candidate gene and whole genome resequencing, gene expression, and epigenetic data sets that promise to capture physiological changes across the life course. In the proposed work, we will provide centralized, integrated archival storage for these multidimensional data sets, create a seamless integration of genetic and phenotypic information at the individual level, and provide a much needed, well documented model of such an integration. We will also work with the National Archive of Computerized Data on Aging (NACDA) to build mechanisms for sharing these data with other researchers in the field. Specifically, we propose to (1) build database modules to house our expanding multi-dimensional genetic and genomic data sets, (2) link these new genetics and genomics modules to our existing database (BABASE) and to each other, to integrate our genetic and phenotypic information, and (3) create a public portal to BABASE that will allow open access to all components of the genetics/genomics modules of the database, as well as open access to key aging- related components of the phenotypic data; this portal will be accessible through NACDA. Our new genetic modules will draw on database module designs pioneered by Chado, a branch of the Generic Model Organism Database project (GMOD). Together, these efforts will provide important archival storage for these valuable data sets, increase the efficiency of data analysis, and promote new, synergistic research directions, including collaborations with outside investigators that will allow us to gain deeper insights into aging in natural mammal populations. In addition, because all the code underlying BABASE and its new extensions will be open source, the proposed work will produce models for how other population studies focused on aging can achieve similar goals.

The objective of this study is to develop novel methods for generating and analyzing genome-scale data from biological samples that have been collected in a noninvasive manner. Noninvasive samples are often the only type of biological sample available for natural populations, especially in endangered or threatened species, but they yield tiny quantities of low-quality DNA. Noninvasive genetic analysis techniques have changed little in the past twenty years, meaning that the genomic revolution has not yet arrived for species for which only noninvasive samples are available. This study will address this problem by producing new lab protocols for increasing and purifying the DNA yield from noninvasive samples to a level appropriate for genomic analysis, and by developing new software to analyze the resulting genomic data. It will validate these approaches by comparing genomic data from noninvasive samples to data from high-quality DNA samples, using data for a known pedigree from the well-studied wild baboons of the Amboseli basin in East Africa.

This project will result in a major leap forward in tools for studying the genomics of many different species and sample types. Publicly available protocols and software will be released, which can be used to investigate evolutionary and population history in species for which such studies were previously impossible. It will also provide societal benefits in the form of tools for assessing the conservation status of vulnerable species. Finally, both graduate and undergraduate students will be trained as collaborators on the project.

DESCRIPTION (provided by applicant): Social adversity, both in early life and adulthood, can have major and long-lasting impacts on human health. Low social status and social isolation in early life have been linked to changes in the immune response and elevated rates of cardiovascular disease later in life, even when status differences are erased. At the same time, social adversity in adulthood - unconnected to any early life experience - has well-documented effects on mortality risk. Thus, traits that are influenced by social conditions early in life reman, at least to some degree, responsive to later social environments. However, the mechanisms that mediate these dual properties-long-term stability coupled with the potential for plasticity an change-remain poorly understood. In particular, we do not understand the molecular mechanisms that translate social experiences across the life course into physiological changes that affect health and disease risk. The goal of the proposed work is to leverage a powerful animal model for social adversity in humans-dominance rank in nonhuman primates-to investigate the relative contributions of early life and adult social status to variation in DNA methylation levels. DNA methylation is an epigenetic mechanism that may serve as an important link between social environment, physiology, and health. However, while this relationship has been investigated in detail for a handful of loci, we do not yet understand its importance genome-wide, or the degree to which changes in DNA methylation in response to the social environment depend on the timing of exposure. Intensively studied primate populations can serve as important models for these questions because known individuals are directly observed from conception to death, and social environmental effects are not confounded by other predictors of health, such as access to health care, diet, or smoking. This application takes advantage of one such population, the well-studied Amboseli baboon population of Kenya, to assess whether and how the relationship between social adversity and DNA methylation changes over the life course. Specifically, we propose to investigate the contribution of social status, in both early life and in adulthood, to patterns of genome-wide DNA methylation in blood. We will investigate targets of DNA methylation that are associated with early life social status, adult social status, or both; if both, we will further test whether these effects act independently. Because variation in DNA methylation levels does not always affect variation in other traits, we will also complement these data with data on gene expression levels from the same individuals, obtained during the same blood draw. The gene expression data will reveal the degree to which DNA methylation patterns that are sensitive to social status also influence downstream gene expression levels. Together, our results will help establish not only whether social status influences DNA methylation, but also the role of different stages of the life course in this relationship and the likelihood that epigenetic mechanisms explain broader relationships between social adversity and health.

Hybridization (genetic mixing between two adjacent species) occurs in many animal and plant species, and is among the most important sources of new gene combinations and new traits in natural populations. Most studies describe hybridization at the population level, rather than describing how hybridization affects individuals. Understanding how hybridization affects individuals will reveal the processes that determine whether genes from one species permanently mix with those of another, or whether this mixing is limited to one or a few generations. Using a wild population of baboons in southern Kenya, this research will provide a detailed description of how hybridization affects individuals. As such, it will be an important model for similar processes in many other organisms, including ancestral humans (who are known to have hybridized with Neanderthals and, before that, with other members of the human lineage). The research involves an international team with substantial participation by women and underrepresented minorities. The team will also contribute teaching modules for middle schools and conduct numerous public outreach activities discussing baboon behavior.

In the first five years of the LTREB project, the Principal Investigator measured the effects of hybridization on a suite of traits that could limit or enhance genetic introgression. The objective of this renewal is to expand this suite of traits, using methods or data that require the longer time horizon afforded by the LTREB mechanism. The specific aims are to (i) identify the sources of the admixture-by-sex interaction previously documented in the maturation schedules of wild baboons, (ii) measure the contribution of genetic admixture to social behaviors that predict male reproductive success, (iii) measure the contribution of genetic admixture to social behaviors that predict female reproductive performance, and (iv) measure the contribution of genetic admixture to social behaviors that predict female lifespan. The proposed work will produce an exceptionally detailed study of the effects of admixture on fitness-related traits in a naturally hybridizing mammal population, which in turn will help shape future hypotheses about mechanisms promoting or inhibiting genetic introgression during hybridization in other species. The data for this project will be stored on a web-accessible PostGreSQL database. A detailed description of the standards for data and metadata can be found in publicly available documents with links at the Amboseli Baboon Research Project website (https://amboselibaboons.nd.edu/ ). All datasets underlying published papers are deposited in the public Dryad Data Repository.

A major goal of evolutionary biology is to understand how genes and environments combine to create the variation we see among animals in nature. Variation in social behavior, in particular, is important to understand, because we know that an animal's social behavior has a major impact on how effectively it copes with its environment. However, social living blurs the distinction between genes and environments because the social environment is (at least partly) determined by the genes of its members. Accordingly, the genes that influence an animal's social behavior include its own genes (direct genetic effects, DGEs) and potentially also the genes of its parents, siblings and social partners (indirect genetic effects, IGEs). Theory has shown that IGEs can profoundly affect how social behavior evolves. However, remarkably few studies have investigated how IGEs contribute to variation in social behavior or whether IGEs affect life history traits and social behavior in natural animal populations, outside of the laboratory. This proposal investigates the role of direct and indirect genetic effects in the evolution of life history and social behavior in a natural population of highly social non-human primates and will thus provide data that can test the theoretical result described above. This will be one of only a handful of studies of both direct and indirect genetic effects on phenotypic variation in the wild, and has the potential to greatly enhance understanding of the evolution of life history and social behavior.

The PIs will use mixed effects linear models (in particular, the 'animal model') in a quantitative genetics approach to measure the direct and indirect genetic variation contributing to life history and social behaviors in the well-studied wild baboons of Amboseli National Park, Kenya. We will also measure the covariance between direct and indirect genetic effects to understand the consequences of this genetic architecture on the phenotypic evolution of these traits. These findings will be communicated to the scientific community and general public through conference presentations and educational outreach. Additionally, this work will provide important training for students and researchers from underrepresented minorities and foster global collaborations between USA, Kenyan and UK institutions.

The male-female health-survival paradox ? the phenomenon in modern human societies in which women experience greater longevity but higher rates of disability than men ? has far-reaching economic and medical implications. The PLs have spent the past five years carrying out the first examination of the health-survival paradox in a nonhuman animal, a population of wild baboons. Their results indicate that male baboons, along with males of several other primate species, have shorter lifespans than females, a pattern they share in common with humans. On the other hand, aging male baboons experience declines in health that are similar to or more rapid than those in females, making them different from humans in this respect. To move forward with comparative studies that can shed light on the health-survival paradox, the PLs propose to develop a more complete picture of commonalities and differences between humans and nonhuman primates in factors contributing to health and survival. To do so, the PLs will build on findings from the current Program Project grant to pursue four Aims. First, in work that cross-links with Project 2, the PLs will investigate sex differences in social status and social connectedness as risk factors for the steeper health declines seen in male baboons than in females. Because male baboons experience much steeper age-related declines in social status and social connectedness than females, these variables ? known to be risk factors for human health and survival ? are implicated as key sources of sex differences in this study system. Second, by observing and measuring rates of wound healing and recovery from illness in the baboons, the PLs will generate unique data for comparison with Project 2 on sex differences in recovery and survival after illness. Third, the baboons are a compelling model for understanding hormone profiles that depend on sex and social status, and this will allow the PLs to gain traction on the question of whether stress hormones mediate the relationship between social factors and survival. Fourth, in collaboration with Project 1, the PLs will use unique comparative data that has been gathered from multiple primate species to develop sophisticated modeling techniques that will allow the measurement of sex-specific mortality patterns with greater accuracy and for a wider range of species than ever before measured. Achieving these aims will provide crucial insight into the underpinnings of male-female differences in health and survival and the health-survival paradox.

Adverse environmental conditions during growth and development can affect physiological function and well-being later in life. This dissertation project will investigate, in a primate model system, whether early-life adversity in primate mothers additionally influences traits in their offspring. Using longitudinal and newly collected data for a natural population of long-lived primates allows researchers to investigate intergenerational effects that may inform evolutionary theory and human health research without having to obtain multi-generation life history data from humans. The project will support international research collaborations, public and K-12 science outreach, and scientific training and mentoring for students from groups underrepresented in STEM fields.

The Amboseli baboons have been under near-daily observation since 1971, resulting in extensive longitudinal demographic, environmental, and behavioral data. The investigators will use these existing data in conjunction with newly collected data on maternal care to test the hypothesis that mothers who experienced adversity during their developmental period provide relatively low quality maternal care to their offspring, leading to deficits in offspring survival. The research will therefore advance knowledge about proximate mechanisms of intergenerational transmission of stress.

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.

SUMMARY Early adversity has powerful effects on development that reach far into adulthood to affect health and survival. At the same time, social adversity in adulthood?particularly social isolation and low social status?is a strong predictor of poor health and survival. These important discoveries, now major topics in social science and medical research, highlight key questions about how early life adversity and adult social adversity are linked, and whether both directly affect survival. Notably, no studies have yet been able to unambiguously link real- time observations of early adversity to detailed data on adult social relationships, health, and survival in the same individuals; the relevant data are exceptionally difficult to collect within any single human population study. A nonhuman primate model is the most expedient way to overcome these barriers, and the time is ripe to develop such a model. Just as primates have long been used as models for cellular, physiological, and molecular mechanisms underlying human health and disease, they can serve as model systems for understanding social and behavioral processes in humans: a number of key studies have demonstrated that important social and behavioral processes are evolutionarily conserved between humans and nonhuman primates. The proposed research will contribute a novel nonhuman primate model of early adversity and lifespan. This proposed study population, a natural population of baboons, has been the subject on continuous research for over four decades and offers prospective, full life-course data, with real-time, direct observations of both early life adversity, adult sociality, and longevity. It sidesteps the complications of health habits and health care access that complicate studies in human populations, and greatly accelerates the timescale for collecting complete life history data, as the lifespans of wild baboons are about 1/3 the length of human lifespans. Three important scientific contributions are expected. First, if the study reveals, as hypothesized, that early adversity and adult sociality both exert independent effects on survival, the work will help shift current research from whether each phase of the life course exerts an influence, to how social behavioral mechanisms contribute to these influences (Aim 1). Second, the proposed study of adult relationships (Aim 2) will provide fresh insight into sources of resilience in the face of early adversity. Third, the proposed model of ?adversity amplifiers? (Aim 3) will formalize an idea that has just begun to crystallize in the adversity literature, stimulating new research avenues. In the aggregate, the work will produce the first complete worked example, in any study system, of the links between early life, adult life, and longevity. The results will help move the field forward by refining critical hypotheses, providing prospective answers to crucial questions, and pointing to the most fruitful avenues for research in diverse human populations.

What are the costs and benefits of living in social groups of different sizes? Theory predicts that living in smaller groups should ease competition for resources within groups. But living in larger groups provides an advantage in competition between groups. These trade-offs between within-group competition (favoring smaller groups) and between-group competition (favoring larger groups) may mean that living in intermediate-sized groups is the best strategy for social species. However, this hypothesis has rarely been tested, and basic questions remain about how competition between individuals and groups affect an individual's energetic condition, and ultimately reproduction and survival. This study will address these questions by analyzing thyroid hormones - a modulator of metabolism and energy balance - in wild primates, in order to understand the relationship between group size, different types of competition, and energetic condition. The research will focus on a wild baboon population in Kenya studied for more than 45 years by the Amboseli Baboon Research Project. To pursue this innovative research direction, investigators will use a repository of approximately 8,000 already-acquired baboon fecal samples collected over a continuous 12-year period from over 200 adult females. Thyroid hormone metabolites will be compared to a rich dataset including information on individual group membership, group size, group movements, reproduction, and life span, among other information, to test the predictions surrounding the benefits of living in groups of varying size. In concert with the research goals, the investigators will build STEM talent and broaden participation of under-represented groups in behavioral ecology and biological anthropology by: (1) providing employment and training for a full-time research technician; (2) mentoring Stony Brook University graduate and Duke undergraduate students; and (3) developing and implementing a sustainable after school program in behavioral science that targets middle school students from high-needs districts. This research is co-funded by the Behavioral Systems Program in the Directorate for Biological Sciences and the Biological Anthropology Program in the Directorate for Social, Behavioral and Economic Sciences.


How resource competition affects survival and reproduction in social mammals is a central topic in behavioral ecology and biological anthropology. This research will address this topic directly by empirically evaluating the tension between resource competition within and between social groups in a wild primate population. To do so, the investigators will quantify the concentration of thyroid hormones in approximately 8,000 already-acquired fecal samples from adult female baboons. The central premise is that variation in thyroid hormone concentrations provides a quantifiable index of individual energetic condition, which will vary as a function of competition for energy resources within and between groups. The resulting data will be analyzed in combination with detailed data on individual females and on social groups. Individual-level data will include social status, age, reproductive state, diet, and agonistic interactions; group-level data will include group size, group-level ranging patterns, intergroup encounters, and group stability. The research aims are to: (1) enhance our existing biological validation of fecal thyroid hormone analysis; (2) quantify the energetic consequences of social rank and group size; (3) assess the energetic predictors and consequences of changes in group size that occur through group fission events; and (4) understand the relative contributions of energetic versus psychosocial processes to variation in female endocrine profiles. This novel approach, which will provide an unprecedented window into the energetic consequences of social rank and group size, has rarely been applied to the study of wild primates and has never been applied to any project of this scale and scope.

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.