Richard Wrangham - US grants

This grant provides support for two years of field research by Dr. Wrangham and his colleagues in the Kibale Forest which is located in southern Uganda. This area has an extremely high density of primates and the reseachers will focus their attention on the common chimpanzee Pan troglodytes . In the two related aspects of the study they will study the process of chimpanzee group socialization and also examine the food calls made by these animals. To accomplish these goals, they will make focal observations on adults encountered within the study area. They will record both activities of individual animals and will also note the composition of the group of which this animal is a member. A series of such observations will allow the reconstruction of the composition, fission and fusion of such groups. The team will also conduct focal tree.watches on fruiting trees and this will allow them to study how different groups and individuals share valuable limited resources. They will record information on the ecology of the entire study area to determine both density and distribution of resources. Finally they will record chimpanzee vocalizations and through a combination of laboratory and situational analysis attempt to determine the number of different calls and the purpose or meaning of each. The goal of this study is to understand the factors which determine how chimpanzees utilize the environment and the relationship between this strategy and group composition. Previous research has made it clear that in different parts of Africa these animals are organized differently and it seems likely that environment plays a role. However no detailed studies have been conducted to answer this question. Closely related to the question of group organization is the issue of cooperation between individuals. Since vocalization sometimes serves to announce the presence of food, through a study of calls, insight will, hopefully, be gained into the kinds of cooperation which take place. This research is important for several reasons. First it sets the context for understanding how humans act. Secondly data collected may help to preserve these rare animals which are endangered in many parts of Africa. Finally, because of the participation of Ugandian students and scientists it should help strengthen the Ugandian scientific establishment and help forge links between Ugandian and U.S. reseachers.

This study will take place at The Detroit Zoological Park and will document the formation of male-female affiliative relationships among chimpanzees during and after the introduction of these animals into a newly built six-acre enclosure, one of the largest in any zoo in the world. This study will collect data to test hypotheses about male-female relationships with particular emphasis on the role of sexual behavior in the establishment of these relationships. %%% The study addresses the question: What are the mechanisms that might lead to the development of stable, long-term bonds between adult males and adult females? This issue has been investigated among baboons, but not previously among chimpanzees. Chimpanzees are one of the most important species for understanding the development of strong affiliative relationships between males and females, both because of their advanced cognitive abilities and because their social structure includes aspects that are strikingly similar to humans.

A new hypothesis has been proposed for the function of conspicuous sexual traits in female primates. The conventional view has been that certain female traits that occur in sexual contexts, such as sexual skin swellings, are designed to attract the attention of or incite competition between males in multi-male species. However, this view does not explain why females in these species would need to advertise their reproductive state so conspicuously or why conspicuous traits would incite more competition among males than would otherwise occur. In contrast, Pagel argues that conspicuous sexual males because they advertise the female's quality or condition. The signals evolve in response to male mate choice and competition among females to attract males (the mirror image of what has been normally accepted). While the female competition hypothesis is the most developed hypothesis to date for the function of conspicuous sexual advertisement in female primates, no tests have been made of its predictions. This dissertation project will examine variation in female sexual traits and their influence on female attractiveness to males in wild olive baboons at Gombe national Park in Tanzania. No study to date has been designed to test the hypothesis that male sexual interest is influenced by variation in any of these female traits in the wild, although it has been apparent that males mate selectively. This study will make a substantial first step towards understanding the evolutionary and social significance of female sexual signals and sexual attractiveness, a topic clearly of vital importance for understanding human evolution. It will also result in the training of young experts in the area of social behavior.

In 1960, Jane Goodall began the first long-term field study of the closest living relatives of humans, chimpanzees (Pan troglodytes), in Gombe National Park, Tanzania to describe their behavior by making extensive observations in their natural habitat. This study, which continues today, has made many contributions to understand chimpanzee behavior and human evolution, and has also inspired people around the world to study science and work toward wildlife conservation. Analysis of the complete observational dataset from Gombe and other field studies, such as the Kanyawara chimpanzee project, has the potential of providing new insights into many unanswered behavioral ecology questions, e.g. the influence of social relationships within the group on territorial behavior.

However, this observational paradigm is extremely labor-intensive and only a small part of the Gombe dataset has been analyzed so far. The goal of this project is to begin developing data analysis tools and techniques to reduce the time and effort required to analyze observation datasets. Expected results include a cartridge for mining concept patterns, a computationally efficient execution environment for concept pattern mining, and spatial semi-supervised learning algorithms to improve classification performance in creating maps. Expected results will not only benefit behavioral ecologists, but also contribute to research in many other spatio-temporal application domains, including location based services, transportation and epidemiology. Dissemination plans include development of instructional tools based on the Gombe data to motivate younger students to learn science and information technology as well as a workshop to increase collaboration between Computer Scientists and Behavioral Ecologists.

Ecology and endocrinology of aggression in chimpanzees.
Richard Wrangham

This study will investigate how aggression among wild chimpanzees is related to age, sex, endocrine status and seasonal variation in energy availability. From 2004 to 2009 the research team will compile a daily record of chimpanzee behavior and ecology within the Kanyawara community of Kibale National Park. The Kanyawara community is a social group of 50 chimpanzees that Wrangham has monitored since 1988, and that are well habituated to the presence of humans. In addition to systematically recording a wide range of behaviors, the research team will also collect urine samples at a rate of about 100 per month. A total of about 11000 urine samples will be available from 1997 to 2009. The concentrations of testosterone, cortisol, progesterone and estradiol will be assayed in these samples.
The researchers will test hypotheses about the relationship of steroid production to behavior (e.g. intergroup aggression, hunting, or status competition), and to behavioral contexts (e.g. mating competition for attractive vs. less attractive females). To do so, they will create a relational database and data management system. This will permit investigations of questions about relatively long-term, infrequent, and complexly related processes in chimpanzee behavioral biology. Long-term questions include how male endocrine status changes with dominance rank, how the frequency of aggression changes with age, or how and why female core areas shift or remain stable over time. Questions about infrequent events include how testosterone output is related to mate-guarding, to border patrols, or to hunting. Complexly related processes include relationships among behavior, party composition, and location. In sum, this research will provide information on a wide range of chimpanzee behaviors, including reproductive strategies, life-histories and social relationships, and will seek to understand them in terms of local ecology and in comparison to other populations.

Chimpanzees will be observed in Kibale National Park, Uganda, to test the hypothesis that daily variation in urinary C-peptide (UCP) levels among adult males is correlated with both food intake and energetically expensive behaviors, such as aggression. The C-peptide molecule is a by-product of insulin synthesis and when excreted in the urine gives an accurate indication of insulin production. Insulin stimulates the uptake of glucose from the bloodstream and thus reflects the availability of energy for the organism.

This study will provide the first direct assessment of the effectiveness of C-peptide, as an index of energy balance in wild primates. Previous assessments have been indirect since they used monthly averages of dietary quality, rather than daily monitoring of individual behavior. This research is designed to explain why dominant male chimpanzees have been reported to have lower UCP levels than subordinates, even though UCP levels track energy intake, being higher when and where fruit availability is greater.

The intellectual merit of this study lies in the possible implications its findings will have for the methodological development of energetics research in field conditions. Non-invasive indices of the energetic condition of primates have always been elusive. C-peptide is promising as an indicator of energetic balance, energy intake, or energy expenditure and this study will assess its value. Understanding the relationship between energy expenditure in male chimpanzees and their dominance rank will also reveal hitherto overlooked energetic costs of dominance in social mammals.

The broader impacts of the project include the contribution to the functioning of Makerere University Biological Field Station. Educational programs will be carried out in local schools to raise awareness and interest in wildlife. This doctoral dissertation research project will contribute to the academic training of a graduate student and the results will be published in peer-reviewed journals.

Bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) are equally related to humans but present contrasting models of the last common ancestor (LCA) of humans and the genus Pan. Bonobos' distinctions from chimpanzees have been argued to be paedomorphic, or juvenilelike, with support for this hypothesis coming largely from cranial morphology but also from certain elements of bonobo behavior. It is currently unknown whether bonobos also exhibit cognitive paedomorphism relative to chimpanzees. This hypothesis will be tested by an investigation of cognitive development in bonobos and chimpanzees. The proposed research will systematically compare infants of both species on a variety of cognitive tasks previously utilized in humans and adult apes. Results will inform the hypothesis that bonobos have undergone selection for a broad spectrum of paedomorphic traits relative to their LCA with chimpanzees. More generally, this work will illuminate how developmental parameters have changed in recent ape evolution, including what features of humans are unique.
This proposal consists of original research synthesizing areas that have not frequently been linked: anthropology, evolutionary biology, and developmental psychology. The results will provide insight into the evolution of human cognition and behavior, the comparative ontogeny of cognition across species, and the effects of shifts in developmental timing on cognitive traits.
This research will be carried out at African ape sanctuaries, contributing to conservation by supplying funding to care for these apes and providing employment in range countries of chimpanzees and bonobos. Sanctuaries are a key conservation resource, providing refuge for apes that otherwise would have been casualties of the bushmeat trade. Ongoing collaboration with Congolese doctoral students will increase the prospects of ape sanctuaries as research sites where local students can develop skills that will allow them to contribute to international scientific dialogue on human evolution and great ape conservation.

Stress, Energetics and the Costs of Reproduction in Wild Chimpanzees
Obtaining accurate, regular assessments of energetic condition is a major challenge in studies of wild mammals. For behavioral ecologists, it is particularly important to record non-invasive measures of condition that impact neither behavior nor energy budgets. Preliminary research indicates that urinary C-peptide, a byproduct of insulin production, is a reliable and sensitive indicator of energy balance in apes. This study will employ non-invasive urine sampling to understand variation in energetic condition in wild chimpanzees (Pan troglodytes schweinfurthii). Measurements of both C-peptide and cortisol (a stress hormone) will be used to quantify the independent effects of energetic and social stress on chimpanzee growth, reproduction and health.
The research exploits a unique 14-year dataset of urine samples and behavioral and ecological data from the Kanyawara chimpanzees in Kibale National Park, Uganda. Together with new, targeted observations, these data will test hypotheses about social dominance and the costs of reproduction. For females, the study will examine such costs over the reproductive cycle, with attention to differences between females living in rich and poor habitats. For male chimpanzees, the study will examine the impact of mating competition on energy budgets and health. The study tests the hypothesis that competition results in increased stress for dominant animals, reflecting the substantial energy costs of male reproduction. Results will shed light on the potential constraints on acquisition and maintenance of high status in this and other species. The broader impacts of this study will contribute to understanding the causes and consequences of energetic and social stress thus furthering conservation goals, particularly when ape populations visited by tourist groups can be regularly monitored. The project will support Ugandan field assistants, a post-doc, and at least one US graduate student. As a long-term research presence, the Kibale Chimpanzee Project will continue to support broader activities in chimpanzee conservation and community development.

All human societies regularly process their foods by thermal and non-thermal means. This feature distinguishes humans from other species, and may even be compulsory from an energetic perspective, given that we possess relatively small molars and gastrointestinal tracts that commit us to an easily digestible diet. Yet the energetic significance of food processing and its evolutionary implications have barely been considered. This study tests the hypothesis that thermal and non-thermal processing lower the metabolic cost of food digestion, known as diet-induced thermogenesis (DIT). Effects will be evaluated for tubers and meat, foods widely exploited by humans and believed to have been critical resources for ancestral hominins. In theory, processing of these foods should result in a loss of structural integrity that lowers DIT due to reduced chewing and gastric effort, as well as increased access by digestive acids and enzymes. Since heat should weaken food structural integrity to a greater extent by gelatinizing starch and collagen, it is further predicted that the effects of thermal processing will exceed those of non-thermal processing. To evaluate these predictions, energy expenditure data are collected via respirometry from subjects before and after standardized meals served raw and whole, raw and pounded, roasted and whole, or roasted and pounded, based on a counterbalanced within-subjects design. Rats will be used as model organisms in the interests of low cost and high control, but a subset of trials will be replicated using human subjects to validate the animal model.

This study will quantify the impacts of thermal and non-thermal processing on DIT, an important factor in energy balance. Results will improve our understanding of the energetic returns of food processing and inform models of hominin transitions toward higher dietary quality. Low DIT has been implicated as a factor in the development of obesity. By determining the effects of food processing on DIT, this research contributes basic data that could help consumers influence the partitioning of meal energy to metabolism versus body stores. Results will thus be communicated broadly to peer-reviewed journals and conferences in anthropology and nutrition, as well as public forums. This doctoral dissertation research project will also contribute to the professional development of a female graduate student.

Of central importance in the science of human biology, as well as that of other species, is full understanding of the complex processes that underlie development, including both the integration of these processes and their evolutionary bases. While experiences during the critical period of childhood are known to have important and lasting effects on future growth, reproduction, health and behavior, the fundamental biology of this system remains poorly understood. This is especially salient for the human species, which has the longest juvenile phase of any animal. By incorporating a phylogenetic approach that examines physical, hormonal, and behavioral development in our closest living relative, the chimpanzee, we can advance understanding of this critical period of development, and determine how different developmental trajectories interact with each other and with the environment to produce adult traits. Comparison of chimpanzees and humans will provide a model for the ways in which biological influences combine with the ecological and social environments to generate adult characteristics, and contribute to understanding when and how unique features of human life history arose in our lineage (such as early weaning, prolonged reliance on parental support, and the adolescent growth spurt).

By using a series of novel, non-invasive techniques, this study will achieve the first detailed documentation of the development of wild chimpanzees, and provide the basis for a comparative, phylogenetic approach to the science of primate, including human, development. Trajectories to be analyzed include physical growth (linear growth, body weight, muscle mass, and tooth eruption), nutrition (behavioral measures of nursing intensity, hormonal measures of maternal and infant energy balance, and isotopic measures of maternal and infant diet), hormones (testosterone, cortisol, estradiol, progesterone, DHEAS and C-peptide), and multiple dimensions of behavior. Hypotheses to be tested will assess how maternal condition, early life nutrition, stress, and related factors influence the timing and rates of development, and the role of hormones in these interactions. The results will be important for understanding sex differences in physiology and behavior. Ultimately, understanding these relationships will allow us to better infer life history shifts associated with changing habitats, ecologies, and morphologies in the hominin evolutionary lineage.

Numerous domestic and international broader impacts are tied to the project. Data generated by the research will be utilized to promote K-12 education in the U.S., working with teachers in both New York and New Mexico to enhance curricula and foster science literacy and appreciation. Education and training of both U.S. and Ugandan undergraduate and graduate students will be fostered through incorporation of these students into the project, and through utilization of the generated data for future research. International collaboration and capacity building, as well as conservation of endangered species, will be promoted by providing economic incentives for protection in Kibale National Park (job creation, training, research fees), supporting anti-poaching and ecotourism programs, and educating Ugandan primary school children about wildlife and habitat conservation.

Zoonotic diseases are those that are transmitted between humans and other animals, and they make up more than half of all infectious diseases in humans. Rodents are one of the richest sources of these zoonoses, yet both theoretical and empirical explanations are scant for why rodents have had such a great impact on human health and why some rodent species readily spread these diseases, while others do not. To better understand the epidemiological relationships that humans have with rodents, this dissertation research seeks to determine whether rodents that live in and around human homes (in an ecological relationship termed "commensalism") pose a greater threat to human health than wild rodents that are not commensal. After determining this, the research team will investigate hypotheses for how the behavior and ecology of different rodent species influence patterns of coexistence with humans. Doing so also will allow the researchers to propose an underlying cause for rodent commensalism, whether mainly for shelter and protection, or for access to food.

In order to maximize both the quantity and quality of data, the research will focus on rural populations in central Kenya, where over twenty endemic rodent species overlap with humans in a single habitat and show varying degrees of infection with zoonotic pathogens. This diversity in rodent species and pathogens is unparalleled within the United States, and it provides an ideal natural setting in which to identify generalizable effects of commensalism on disease transmission. To determine differences in infection due to commensalism, the doctoral student researcher (Collin McCabe, under the supervision of Dr. Richard Wrangham, Harvard University) will capture rodents within homes and in nearby undisturbed habitats. Blood will be drawn from these animals, and these samples will be sent to a lab in the United States for zoonotic pathogen detection. The researchers will then assess the risk-taking behavior of the animals and also will evaluate their diets to determine the most likely explanation for these rodents' cohabitation with humans.

By defining the patterns of infection and exposure among free-living rodents and humans, results of this research will suggest whether wild or commensal rodents present a bigger disease risk to humans, and by understanding the factors that influence commensalism, public health agencies can focus control efforts on the most likely areas of human-rodent overlap. In today's highly connected world, the health concerns arising from new disease outbreaks are truly global. Thus, by contributing to awareness and control of zoonotic outbreaks abroad, this study also will contribute to American health security.

DESCRIPTION (provided by applicant): While it is clear that lifespan was extended during human evolution, there is remarkably little data available to assess the specific ways by which this remarkable change in life history came about. This missing information could importantly inform the understanding of how modern lifestyles, in interaction with our evolved biology, produce the health outcomes observed in developed countries. A major limitation at present is a dearth of data on the aging process in humans' closest evolutionary relative, the chimpanzee. The current study would be the first to gather comprehensive data on aging in wild chimpanzees, whose health has not been manipulated by humans during captive management or biomedical experimentation. Like humans during most of their evolutionary history, wild chimpanzees experience frequent nutritional stress and high rates of infectious disease and these processes - little studied in modern aging research - are expected to have shaped species-normative life history strategies. The project entails non-invasive collection of urine and feces from approximately 245 wild chimpanzees (Pan troglodytes) for a broad range of health biomarkers, in additional to observational research for observed morbidity, locomotor proficiency, and social behavior. New data collection will complement and extend existing long-term demographic data, as well as individual histories of social interaction and reproductive effort. The wild data will be supplemented by additional blood-based biomarkers obtained during routine veterinary immobilizations of approximately 240 semi-free ranging chimpanzees in African sanctuaries. The project integrates investigators from major studies of health and aging in human foraging populations, and the central aim (1) of the project is to perform structured comparisons of health and aging between humans and chimpanzees. To further this goal, the additional project aims focus on key variables that are expected to shape senescence, and which are associated with prominent behavioral differences between species: (2) sex differences and the allocation of reproductive effort across the life history, (3) stability of accss to energy, and (4) social status and support. Information gathered in pursuit of these aims has specific relevance to prominent focuses of human aging research: the gender morbidity-mortality paradox, caloric restriction, and the influences of chronic stress and social subordination.