Jacinta Beehner - US grants

Humans routinely assess other people by relying on information gained during previous experiences with a particular individual (?individual recognition?). Indeed, individual recognition is the primary means of assessment for most primate species. However, a growing body of evidence indicates that humans also use physical characteristics (?quality signals?) as a way to evaluate others ? particularly in the context of competition and mating. One reason why humans might utilize quality signals is because they live in extremely large social groups where they frequently encounter individuals they do not recognize. However, this hypothesis is difficult to test because quality signals are rare among primates, and little is known about the function and use of signaling in non-human primates. Thus, the main objective of this research is to determine how primates living in large groups ?size up? potential rivals and mates ? a task that involves mapping the boundary of where individual recognition ends and where other short-hand means of assessment begin. The subjects for this research are wild geladas (Theropithecus gelada), a monkey that lives only in the highlands of Ethiopia. Geladas are an ideal species for this research for two reasons. First, while the vast majority of primates live in small groups where individuals recognize every group member, geladas (like humans) live in extremely large groups where individual recognition may not extend beyond a small subgroup. Second, male geladas are unusual among primates in having 2 conspicuous traits that may serve as quality signals, a red patch of skin on the chest and neck, and ritualized display vocalizations. By combining behavioral observations, experimental playbacks, and laboratory analysis of fecal steroid hormones, this research addresses 3 questions: (1) What are the limits of individual recognition in gelada society? (2) For recognized individuals, do they base reproductive decisions on this information? (3) Alternatively (or additionally), do geladas use quality signals, such as chest color or vocal displays, to evaluate potential competitors or mates?

The PI and co-PI of this project are committed to integrating research goals with education and conservation at several levels. First, over the course of this three-year project, a post-doc will receive training in playback experiments and hormone analysis, 4-6 graduate students will gain summer field experience, and 6-8 undergraduates will gain experience analyzing data for senior theses. Second, it is expected that 1-3 Ethiopian graduate students in primate behavior will join the project. Third, an Ethiopian counterpart will be sponsored for graduate training in wildlife management. Finally, this project's research presence in the Simien Mountains National Park (currently on the list of World Heritage Sites in Danger) is assisting conservation efforts. Conservation projects that have been initiated thus far include: a census of geladas living in the area, a survey for tourists on park conservation, and a survey for the local people to gauge the degree of human-wildlife conflict. Both the PI and co-PI will continue to dedicate a fraction of their field time to conservation efforts in the area.

Among mammals, females generally invest more than males in each reproductive event -- an imbalance that often results in different reproductive strategies for males and females. The typical male strategy is to mate with as many females as possible while females are generally more "choosy" and will only mate under favorable social and environmental conditions. Possibly the most salient example of a male reproductive strategy is infanticide - when a male kills a female's unweaned offspring (sired by another male) to hasten her return to a fertile state. In turn, to protect their reproductive effort, female mammals often develop counterstrategies to infanticide such as forming defensive alliances with other individuals in their social groups, producing deceptive sexual behavior and sexual swellings to mimic the signs of fertility, spontaneously aborting a pregnancy, or prematurely weaning dependent young. Anecdotal evidence on wild geladas (Theropithecus gelada), a close relative of baboons, suggests that infanticide following male takeovers may be a threat for females with dependent offspring. However, as yet, female reproductive counterstrategies in geladas have never been examined. This project aims to investigate the function and underlying physiology of female reproductive strategies in geladas, to answer the question: does intersexual conflict exist in geladas? The first objective is to describe the normative patterns of gelada reproduction in terms of gonadal hormones, sexual swellings, and female reproductive behavior. The second objective is to investigate the functional significance behind the physiology, sexual swellings, and reproductive behavior of female geladas following male takeovers. In other words, this research will determine whether infanticide is a threat to female geladas and whether females have developed counterstrategies as a result.

This research is unique in two ways. First, it explores the potential for intersexual conflict to exist in geladas from both mechanistic and adaptive approaches. Female physiological profiles will reveal whether females perceive male takeovers as a threat and whether female sexual swellings are deceptive or not. Field observations will provide the behavioral context with which to interpret the hormonal data. Together, the hormones and behavior yield a more complete picture of what is going on. This is the first study to investigate the hormones and behavior surrounding female reproductive strategies in primates. Second, infanticide will be investigated from the female's perspective. While infanticide has been investigated in a variety of species, research has strongly focused on the costs and benefits for males. Further documentation of female reproductive strategies and counterstrategies in primate species will contribute towards a better understanding of intersexual conflict.

Data from this work will have important conservation implications. Geladas are an endangered species and improved understanding of their reproductive behavior can help breeding efforts in captive settings.

The physical, behavioral and ecological diversity of baboons (genus Papio) makes them a fruitful source as analogies for understanding early human evolution. This project investigates a widespread but little known species, the kinda baboon (P. kindae), and probes the physiological and genetic bases of its distinctive behaviors and physical features. Besides being unusually small and juvenile in appearance, kinda baboons appear less sexually differentiated than other baboons. Behaving like females of other species, adult male kindas frequently initiate long grooming sessions, while females often give alarm barks, which is normally a male baboon activity. Unexpectedly, kinda baboons hybridize with neighboring chacma baboons (P. ursinus) which are almost twice their size, and are behaviorally more typical. This research project traces the causes of these species differences from the level of observable behavior and anatomy, through the level of development and hormonal control, to the level of the genome. Over 200 kinda, hybrid, and chacma baboons are trapped, sampled, and released unharmed in Kafue National Park, Zambia. Basic biological data such as weight and body measurements are collected along with blood samples. Specialist labs investigate these blood samples for the hormones and other biologically active components that influence growth, sexual differentiation, and behavior, and produce a high-resolution map of the kinda genome. Physiological differences that consistently distinguish kindas can then be tracked to the genetic level, by comparing fast-evolving candidate regions in kindas with homologous regions in other baboon species.

The project is innovative in combining proven, comparatively low-tech field techniques with cutting edge technology in genomics and hormonal physiology. Most immediately, it fills a major gap in our knowledge of a key primate genus. In the long term, it provides insights into behavioral variation and evolution in other species, including humans. In the wider sphere, the project will train graduate students, further scientific collaboration with Zambian Wildlife authorities, and promote the status of baboons in wildlife tourism.

Strong male bonds are rare among primates, especially for female-bonded species. Thus, the relationship between male bonding and reproductive strategies remains largely unexamined in female-bonded species. Geladas (Theropithecus gelada) provide an ideal model for understanding how male bonds influence male reproductive trajectories in a female-bonded species. Prior to acquiring reproductive access to females, "bachelor" geladas live in cohesive all-male groups. Eventually, males graduate from these groups to gain sole reproductive access to a group of females (one-male unit). Bachelors acquire one-male units using one of several strategies: (1) directly overthrowing the leader male, (2) submissively entering a unit and attempting to pare females away from the unit over time, or (3) capitalizing on the chaos of a recent takeover to opportunistically mate with females. Additionally, bachelors have been observed to cooperate in attempts to overthrow leader males and enter one-male units with former members of their all-male group - yet only one male eventually reaps the reproductive benefits. This project investigates the behavioral and hormonal factors that shape the reproductive trajectory of gelada males as they move from an all-male group to a one-male unit. The researchers will(i) describe the social interactions among bachelors within their all-male group; (ii) determine the behavioral and hormonal factors that influence bachelor participation in takeover attempts of leader males, and (iii) determine whether bachelor quality predicts a reproductive strategy. Behavioral data and noninvasive fecal hormone sampling will document the reproductive trajectories of male geladas. Additionally, digital photographs will be taken of male chest patch color - a feature that may indicate male quality - to document changes in color as males move from their bachelor groups to one-male units.

Results from this research will inform conservation decisions regarding these rare primates, and the investigator's presence in the Simien Mountains National Park help deter illegal activities in this World Heritage Site that is in danger. This project provides income and training to local Ethiopian field assistants and the co-PI has arranged to explain gelada behavior to high school students in several U.S. states.

Geladas (Theropithecus gelada), like humans, live in unusually large social groups with numbers that exceed 1000 individuals. Unlike humans, however, the dominant males in gelada society do not recognize other males around them - even males that they encounter on a daily basis. This creates a socially and evolutionarily (fitness-related) significant set of limitations for males competing for mates; mainly, how to assess rivals prior to engaging in costly forms of competition. Species that do not use individual recognition for assessment typically use short-hand proxies; i.e., particular physical features or other characteristics ("signals") which are useful for ascertaining the competitive abilities of potential rivals. Although such signals in primates are rare, the unusually large groups found in gelada society may have favored their evolution through a form of natural selection referred to as "sexual selection."

Research by doctoral student Marcela Benitez (University of Michigan), under the supervision of Dr. Jacinta Beehner, will examine one such putative signal for male geladas living in the Simien Mountains National Park, Ethiopia - a loud vocalization used in male displays (i.e., "loud calls"). Establishing whether loud calls are evolved signals requires establishing the following: (1) that variation exists in loud calls across males of different quality, (2) that males can use these calls to distinguish between high and low quality males, (3) that males then base challenges on these calls, and (4) that males with high quality calls have higher fitness (reproductive success). To address these predictions, this interdisciplinary research will combine acoustic, experimental, hormonal, and observational analyses on known individuals that have been followed continuously for the past six years. As such, the research represents one of the most comprehensive studies of what are theoretically termed "sexually-selected signals" (i.e., those evolved through male-male reproductive competition) with potential fitness consequences in a primate.

This research is part of a long-term project that is committed to increasing conservation awareness and scientific education, both in the U.S. and in Ethiopia, through collaborative research and educational presentations to local people and eco-tourists in Ethiopia. The doctoral student Co-PI, a member of an underrepresented group in science, will incorporate the research into her bilingual website for childhood educational outreach, promoting engagement with the sciences by US children.

One intriguing hypothesis about the origins of human language is that it emerged as a 'social tool,' facilitating our abilities to maintain relationships with an increasing number of people (the "social grooming hypothesis"). The basic idea is that social grooming (which facilitates a bond with only one individual) is replaced by vocal 'grooming' (which facilitates bonds with several individuals, simultaneously). Indeed, social bonds have adaptive value for both humans and non-human primates. Thus, if vocal contact represents an efficient way to maintain relationships, then selection should favor its development. Despite a great deal of theoretical support, however, the social grooming hypothesis has yet to be tested empirically. Geladas provide an excellent model to test this because they are highly social, exceptionally vocal, and uniquely time-constrained because they must spend much of their day foraging on grass. This research by doctoral student Elizabeth Johnson (University of Michigan), under the supervision of Dr. Jacinta Beehner, will explore the strategies that female geladas employ to maintain their social networks, with a specific emphasis on when vocalizations are used, the responses they elicit, and whether such vocal contact supplements or replaces social grooming when time budgets are particularly strained. By utilizing a combination of methods, including behavioral observation, social network analysis, analysis of 'stress' hormones, and acoustic analysis of recorded vocalization, this research will elucidate one possible route by which human ancestors may have maintained social bonds, allowing for larger groups and greater group cohesion.

Results from this study not only contribute to a better understanding of female gelada social relationships, but also provide a comparative dataset for on-going collaborative projects on closely related species (e.g., anubis and hamadryas baboons). Further, this research extends beyond academia, raising awareness about the study site (the Simien Mountains National Park of Ethiopia, a World Heritage Site in Danger) and the study species, an endemic species to the highlands of Ethiopia with a conservation status labeled as "Threatened" by the IUCN Red List. Finally, this doctoral dissertation research project contributes to the long-term viability of the park by hiring a local field assistant (providing both employment opportunities as well as continuing education for these young adults), working closely with park officials, and providing educational lectures to Ethiopian nationals.

Very little is known about how complex mammalian societies develop from the interaction of individual social behaviors. In dynamic/fluid social groups, two critically important questions are: what brings smaller core groups together, and the flip side of what splits them apart? The research in this study will study the highly social Old World Monkey geladas (Theropithecus gelada). Geladas are an excellent model system to address this question as they have complex social groups and are easy-to-observe terrestrial animals that live at high densities. This research uses a combination of demographic and behavioral data, social network analyses, and population genetic data to pinpoint the individual gelada behaviors that contribute directly to their social complexity. Additionally, using behavioral, life-history, physiological, and reproductive measures, this research will measure the costs and benefits of different social interactions. The results of this research will establish not just how complex societies emerge from individual behaviors but also why the individuals exhibit those particular behaviors, representing a critical step in understanding how some animals, like humans, moved from simple to complex societies.

The long-term project has and will continue to: (1) strengthen collaborative relationships both within the U.S. and between the U.S. and Africa; (2) provide training to American and Ethiopian undergraduate, masters, and Ph. D. students; (3) assist conservation efforts in Ethiopia through the preservation of national parks, (4) provide outreach both within Ethiopia (offering regular seminars on gelada behavioral ecology to both Ethiopian nationals and international tourists), and within the U.S. (through interactive lectures for K-12 students). Specifically, the members of this project have spear-headed Michigan Primate Outreach, which involves a series of age-appropriate lectures on primates and conservation for students of all ages (see project website for all outreach activities: http://www.umich.edu/~gelada/UMGRP/Home.html).

Current understanding of the long-term effects of prenatal hormone exposure on offspring fitness in natural populations is extremely limited, particularly in viviparous species. The proposed research investigates the fitness consequences of prenatal androgen exposure in a long-lived mammalian carnivore, the spotted hyena. Wild hyenas are studied in Kenya to document correlates and consequences of naturally-occurring variation in early androgen exposure. Cubs born to mothers with known concentrations of androgens during pregnancy are followed into adulthood to test a hypothesis suggesting that androgen-induced variation in cub behavior and morphology is associated with variation in fitness. Two other competing hypotheses are also evaluated, each suggesting different extents to which opposing hormone effects might constrain adaptive evolution. This work will permit uniquely integrated study in long-lived mammals of the development of hormonally-induced traits, from their induction in the womb to their consequences in natural populations. It will be important for understanding more broadly the role of prenatal androgen exposure in the generation of variation in behavior and morphology, and the role played by androgens in the evolution of mammalian life histories. This research crosses disciplinary boundaries and offers unique and highly valuable international training opportunities for American students. The work also trains Kenyan students, and supports Masai students in local elementary schools near the study site. In addition, project personnel work closely with the public media in the USA and abroad, maintain an educational website, and give many lectures each year to lay audiences. Finally, via a web portal this research makes available to other researchers and the general public core data tables in a database that documents hyena behavior, demography, and physiology at the study site since 1988. This project is jointly supported by the Animal Behavior Program and International Science and Engineering.

Some studies have shown that high levels of stress hormones in animals are linked to lower reproductive success and survival ("fitness"). Other studies have found that higher stress hormone levels may be beneficial. In wild animal populations it is often hard to measure fitness and correct for other factors that affect hormone levels. This RAPID project will support immediate collection of stress and survival data for several capuchin monkey groups in Costa Rica. These monkeys are currently experiencing the environmental effects of a strong El Niño climate pattern. The opportunity to study a well-monitored monkey population during a stress event (El Niño) that affects all individuals is rare. The project will provide new data on how an individual's past and present hormone levels relate to their fitness. The researchers support graduate training of individuals from underrepresented groups in the STEM sciences. The project also includes science outreach activities in Costa Rica and the United States, and primate conservation efforts.

This project will test the cort-fitness hypothesis, which suggests that higher glucocorticoid hormone levels will be associated with reduced fitness. Currently, a very strong El Niño event is causing unprecedented mortality among a habituated, well-known population of white-faced capuchin monkeys (Cebus capucinus) at Lomas Barbudal in Costa Rica. This event presents the opportunity to test whether elevated glucocorticoids increase or decrease survival in wild capuchin monkeys subjected to a catastrophic stressor that affects all individuals. Longitudinal behavioral and fitness data and fecal measures of glucocorticoids will allow for an individual-level approach, correction for several other variables known to affect glucocorticoids in wild primates, consideration of past and present hormone levels for the same individual and in comparison with others, and assessment of infant mortality and maternal hormone levels.

In nonhuman primates a range of male behaviors are observed that relate to male success in siring offspring. This doctoral dissertation research project examines reproductive payoffs of different male strategies (aggressive versus affiliative) in wild geladas (primates). Results from this study provide valuable insights about the evolution of male reproductive strategies and will enhance understanding about the adaptive significance of male-female social bonds in a long-lived primate species. While conducting the proposed research, the doctoral student will continue to work with K-12 students from underrepresented communities to foster excitement about science and research and give talks about primate behavior and evolution at local elementary schools. Additionally, the doctoral student will continue training undergraduate students in the laboratory throughout her dissertation research and mentor women from groups underrepresented in primatology.

This research investigates how different male behavioral strategies affect reproductive success in geladas. Male geladas gain reproductive opportunities by becoming the dominant leader over a family of multiple females and their offspring. Male reproduction is thus a function of the number of fertile females in the group combined with how long he remains the dominant leader (tenure length). The proposed project will use long term data (collected over 13 years) in combination with detailed behavioral, hormonal, and paternity data from individually known leader males to assess which factors contribute to male reproductive success. First, the investigators will measure reproductive success by assigning paternity through genotyping all leader males and infants in the project. Second, they will quantify physical attributes that could affect reproductive success in geladas. These include: i) body size (measured through laser photogrammetry), ii) chest patch redness (measured by comparing photos of gelada chest patch against a standard color checker chart), and iii) testosterone levels using fecal samples collected from individual leader males (measured through a biotin labelled enzyme-immunoassay). Third, the investigators will assess what social strategies males employ to increase reproductive success by quantifying male-female social relationships through behavioral observations and recording the occurrence of infanticide.

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.

Water insecurity is a worldwide problem and can be a major stressor that negatively impacts mental and physical health. Despite this burden, the connections between perceived water insecurity, psychological stress, and biological responses are not well understood. This doctoral dissertation project incorporates a biocultural approach to examine whether objective and/or perceived water insecurity are socio-environmental exposures that impact human biology. The study focuses on the experiences of women who often must cope with the burden of water insecurity, examining relationships between stress, resource insecurity and health that may be variable and mediated by culturally specific practices. The project findings may aid in the development of future policies addressing environmental and social inequality. Results from this research are shared with national and international communities through outreach activities, which strengthens international collaborations and can inform future studies exploring the short and long-term effects of resource insecurity. <br/><br/>This study builds upon biocultural studies of embodiment and health, proposing that the subjective perception of resource insecurity, in this case water insecurity, and the practices derived from it are key factors contributing to health disparities. This project investigates the connections between perceived water insecurity, psychological stress, and DNA methylation in stress-related genes by comparing women from water-secure and water-insecure neighborhoods in a rapidly growing megacity. Perceived water insecurity and perceived stress are gauged using interview questionnaires. Saliva samples are collected to measure DNA methylation in stress-related genes. This mixed-methods approach can provide a critical biocultural understanding of the extent to which perception, anticipation, or fear of water insecurity may impact mental and physical health.<br/><br/>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.