Maternal predictors of infant developmental trajectories in olive baboons (ASUF 30007670) Maternal predictors of infant developmental trajectories in olive baboons Proposal Patterson Maternal predictors of infant developmental trajectories in olive baboons RESEARCH OBJECTIVES AND QUESTIONS I propose to investigate the influence of maternal signals on infant developmental trade-offs in a population of wild olive baboons in Laikipia, Kenya. Early life experiences exert important influence on development and the mother is the critical early environment for mammalian infants. However, it is not yet clear how maternal signals are shaped and how infants use signals to navigate developmental trade-offs. I will measure behavior, social relationships, body size, and physiology of mothers and infants to answer a series of questions. First, what predicts variation in maternal signals? Second, how do infants respond to maternal signals? Third, how do infants navigate developmental trade-offs? RELEVANCE TO HUMAN ORIGINS Much of the variation in human life history has been attributed to developmental plasticity tied to the environment and this plasticity is hypothesized to have played an important role in the evolution of human life history (Kuzawa & Bragg, 2012). Previous research on humans has been handicapped by the difficulty of collecting repeated physiological and growth data from individuals and the difficulty of obtaining systematic data on behavior and the mothers relationship to the environment. Because the evolution of signals and developmental trade-offs do not fossilize, the evolutionary history of these systems is difficult to examine without a cross-species comparative lens. By studying wild baboons, I will be able to collect repeated physiological, behavioral, and growth samples using noninvasive and objective methodologies. Access to long-term ecological and demographic data will provide a means to measure the mothers early life adversity and her relationship to the environment across her life. Ecological variation at the study site will provide insight into how high sugar diets and predictable food availability traits that characterize changes across human evolution influence maternal signals and investment, the timing of critical windows of sensitivity, and infant phenotypes. BACKGROUND Early life experiences can have substantial influence on development and adult outcomes. Experiences such as resource shortages and early life adversity shape a diversity of traits ranging from health to sociality to reproduction (Gluckman et al., 2008; Lea et al., 2015; Nussey et al., 2007; Tung et al., 2016). For example, placental size is linked to heart disease and diabetes risk in humans (reviewed in Rutherford, 2013). Wild female yellow baboons (Papio cynocephalus) that experience greater early life adversity are less socially connected as adults than females that experience less early life adversity (Tung et al., 2016), and sociality in turn is linked to longer longevity (Archie et al., 2014) and lower infant mortality (Silk et al., 2003). The mother is a crucial component of the early life environment for all mammals. However, the period of dependence is prolonged among primates (Charnov & Berrigan, 1993), and this suggests that the maternal environment is Proposal Patterson particularly important for primate development. The maternal environment influences offspring growth, immune function, health outcomes, physiology, cognitive development, dispersal patterns, and reproductive strategies in a variety of taxa (Blomquist, 2013; Catalani et al., 2011; Groothuis & Schwabl, 2008; Guenether et al., 2014; Langley-Evans, 2007; Machado, 2013; Mateo, 2014; Mousseau, 1998). Mothers provide necessary nutrients and immunological factors for their infants (Hinde & Milligan 2011), and they also provide information to their infants about maternal condition and the quality of the environment (Wells, 2003, 2007ab, 2010, 2014). This information is communicated via physiological and behavioral signals. For example, maternal glucocorticoids (GC) hormones that are released following the activation of the hypothalamicpituitary-adrenal (HPA) axis and play an important role in mobilizing energy and metabolic resourcesare transferred from mother to offspring across the placenta and through mothers milk (Meaney et al., 2007; Pacha, 2000). Offspring use these maternal signals to guide their development in an adaptive way (e.g. Dantzer et al., 2013). For example, squirrel pups (Tamiasciurus hudsonicus) that experience high levels of maternal GCs, a signal of high population density, accelerate growth and improve their chance of survival (Dantzer et al., 2013). I propose to examine the impact of maternal signals on three developmental dimensions: growth, activity levels, and physiology. I aim to answer the following questions: What predicts variation in maternal signals? How do infants respond to maternal signals? How do infants navigate developmental trade-offs? Savanna baboons provide a useful model for studying the link between maternal signals and infant development. Recent work demonstrates that baboon mothers early life experiences exert important effects on their development, longevity, and sociality (Lea et al., 2015; Tung et al., 2016). Baboon mothers who are more socially integrated in their groups have higher survivorship among their offspring (Silk et al., 2003; Silk et al., 2010). The proximate factors that underlie this effect have not yet been identified, and it is not known how mothers early life experiences and current condition influence maternal signals or offspring development. Olive baboons (Papio anubis) provide a particularly interesting species for investigating how maternal signals influence infant development, activity, and physiology. The strong, differentiated social bonds formed by mothers create an opportunity for examining how social support provided by close female kin and male partners affect maternal signaling and infant development. Like other savanna baboons, females form strong ties to close female kin (mothers, daughters, and sisters; Silk et al., in review). Female olive baboons also form strong and lasting ties to adult males (Silk et al., in review; Smuts, 1985; Strum, 1975). Females social ties may buffer the effects of challenging environmental conditions. Previous research has been handicapped by the difficulty of measuring individual growth trajectories. We will take advantage of newly developed methods to measure body size noninvasively with photogrammetry. A digital SLR Proposal Patterson camera will be fitted with two parallel lasers, and the laser projections will create a measurement scale that can be used to assess stature (Bergeron, 2007; Rothman et al., 2008). Sequences of photogrammetric measures on known individuals can be used to estimate growth rates. Our study site provides an unusual opportunity to monitor animals with substantially different foraging ecologies. A New World cactus, Opuntia stricta, has invaded a portion of the study area. For groups that range in areas where O. stricta is common, its fruit has become an important component of the baboons diet (Strum et al., 2015), and reduced seasonal variability in food availability. Changes in the nutritional regime have influenced female fertility. Two of our study groups rely heavily on O. stricta, and interbirth intervals in these groups have decreased substantially (unpublished data, UNBP). I will collect data from two troops that feed heavily on O. stricta and one troop that occupies a range with substantially less O. stricta. This ecological variation will amplify variation in maternal condition, and this will enhance my ability to detect variation in maternal signals and evaluate the impact of this variation on infant phenotypes. SPECIFIC OBJECTIVES AND HYPOTHESES Hypotheses to be tested Q1: What explains variation in maternal signals? Hypothesis 1: The mothers relationship to the environment influences her behavior and physiology, which act as signals to guide infant development. Q2: How do infants respond to maternal signals? Hypothesis 2: Infants use maternal signals to guide developmental trajectories. Hypothesis 3: The strength of infant response to maternal physiological signals will be a function of timing and frequency of nursing. Q3: How do infants navigate developmental trade-offs? Hypothesis 4: Infants face trade-offs between growth and levels of activity. METHODS AND ANALYSES Study site. The field portion of the project will be conducted from October 2016 December 2017 in Laikipia, Kenya, in collaboration with the Uaso Ngiro Baboon Project (UNBP) directed by Dr. Shirley Strum. UNBP has collected demographic and ecological data on a number of olive baboon groups for over 40 years. I work with the Comparative Analysis of Baboon Sociality project (CABS), directed by Dr. Joan Silk, which began studying two groups monitored by the UNBP in September 2013, with a focus on the structure and function of social bonds. This project will extend research to a third social group monitored by UNBP. I will follow 20 mother-infant pairs that are members of two groups that range in areas with a high density of O. stricta and 20 mother-infant pairs that belong to a group that ranges in an area in which the plant is still uncommon. All baboons in the focal troops are individually recognizable and habituated to observers working on foot. For the current project, I will collect behavioral, physiological, and photogrammetric data on mothers and their infants. UNBP records of female reproductive condition (assessed daily), maternal condition (weekly), rainfall (daily), and herbaceous biomass (monthly) will supplement my data. Proposal Patterson Behavioral data collection. Focal animal samples (Altmann, 1974) will be conducted on mothers and infants. Three research assistants will conduct focal samples on mothers in all three troops and I will conduct the focal samples on infants. Inter-observer reliability will be checked on a monthly basis. Focal observations last 15 minutes and are conducted approximately three times per week on mothers and four times per week on infants from birth until mothers next birth (IBI N = 97, mean = 572 days, standard deviation = 179). The focal data on mothers will be used to extract the following measures: time in one meter proximity to the infant, time infant is carried, time on nipple, time infant is groomed by mother, and the rate of aggression toward infants, rejections, and restraints. The focal data on infants will be used to assess responsibility for maintaining proximity within one meter, the rate of distress behavior, and the proportion of time spent socializing (grooming and playing). Five types of play behavior will be recorded continuously: active play, object play, noncontact social play, contact social play, and chase play (Fairbanks, 2000). Maternal Characteristics. Maternal social capital will be measured with current dominance rank determined with elo-ratings (Neumann et al., 2011), count of close maternal kin (mother, daughters, sisters), strength of social bond with the mothers top male partner (dyadic sociality indices: Silk et al., 2013), and social connectedness (social network analysis metrics: Farine & Whitehead, 2015). Following Tung et al. (2016), mothers early adversity will be measured as a cumulative count of the following: droughts during the first year of her life, group size at birth, presence of competing younger siblings (those born within 1 year of mothers birth), loss of her mother before age at menarche, and her mothers dominance rank at birth. Hormone sample collection and assays. Fecal samples for GC analysis will be collected from mothers once per week during gestation and lactation. Fecal samples for GC analysis will be collected from infants two times per month from 4 months of age through mothers next birth. During the first 3 months of life, when samples are very difficult to collect, we will obtain samples ad libitum. This level of sampling will provide detailed GC profiles across the study period. Hormones will be extracted from feces collected in the field using a method described by Beehner and Whitten (2004). Fecal samples will be mixed thoroughly in a methanol/acetone solution, and immediately homogenized using a battery-powered vortexer. The dry weight of all fecal samples will be determined later (0.001 g) using a battery-powered, portable scale. Approximately 7 h after collection, 4.0 ml of the fecal homogenate will be filtered through a syringeless Whatman filter, and the filter will be subsequently washed with methanol/acetone. We will then add distilled water to the filtered homogenate, mix the solution, and load it onto a prepped, solid-phase extraction cartridge (Sep-Pak Plus, Waters), followed by a sodium azide solution as a wash and preservative. All samples will be stored dry on cartridges in separate sealed bags with silica beads at subzero temperatures (-10C) until transported to the United States for analysis. I have permission to be trained and conduct hormone analyses in the Core Assay Facility directed by Dr. Jacinta Beehner at the University of Michigan. Proposal Patterson Body size. I will use noninvasive photogrammetric methods to measure body size (Bergeron, 2007; Rothman et al., 2008). Mothers will be photographed monthly across gestation and lactation to capture changes in body size. Infants will be photographed once a week from birth through the end of the study period. Photographs will be taken while subjects are standing on level ground with the longitudinal axis of the body perpendicular to the photographer. Analyses of growth photographs will be conducted at Stony Brook University in the laboratory of Dr. Amy Lu. ANALYSES Statistical analyses will include multiple data points from each mother and infant. To account for non-independence from this resampling, I will employ mixed models with individuals treated as random effects. H1. To assess factors that influence variation in maternal signals, I will construct a model with monthly concentrations of maternal GCs as the output variable and another model with monthly rates of maternal care behavior as the output variable. The independent variables in these models will include: monthly rates of predator, inter-troop, and human encounters, adversity index, social capital measures, maternal parity, and maternal rank. H2-3. To investigate how infants respond to maternal signals, I will run a mixed model with each infant developmental trait (growth rate, percent time active, and GC concentrations) as the output variable. The independent variables will include: maternal GC concentrations, frequency of maternal care behaviors, time of signal (gestation, early, mid, or late lactation), the interaction between time of signal and maternal GCs, the interaction between nursing frequency and maternal GCs, infant sex, maternal parity, and maternal rank. H4. To examine how infants navigate trade-offs between growth and active time, I will run a mixed model with growth rate as the output variable. The independent variables will be active time and infant sex. EXPERIENCE AND PRELIMINARY DATA My past research experiences have prepared me to carry out this study. I worked at the proposed field site as a research assistant on the CABS project from January 2014-July 2014, and returned to the field site in 2015 to conduct pilot work for the current project. I gained important knowledge about the research protocol, the region, and the types of data collection that are feasible. CABS data provide preliminary results that inform the current research project. The proportion of time that infants were on the mothers nipple, carried by, and in proximity to the mother decreased steadily over infancy (Fig.1). Mothers with male infants spent more time nursing, carrying, and in proximity to their infants than mothers of female infants (proximity: F(1, 37) = 6.244, p = 0.017; carrying: F(1, 35) = 5.018, p = 0.032; nursing: F(1, 26) = 2.321, p = 0.140) (Fig.1). Interbirth intervals (IBIs) following sons are significantly longer than those for daughters (F(1, 32) = 5.204, p = 0.029). Maternal age also influences IBIs with older mothers generally experiencing longer IBIs after surviving births (F(1, 48) = 3.766, p = 0.058). During 2015 and 2016, the number of encounters with Proposal Patterson predators, other baboon groups, and humans varied considerably from month to month (predators: 1-6, troops: 1-16, humans: 2-35). This variation will be important for my analyses of predictors of maternal signals. Females also vary in the nature of their associations with adult males. Most females form strong ties to selected adult males, and these ties extend beyond the neonatal period (Silk et al., in review). However, the strength and stability of ties to preferred males varies across females. In addition, the number of close female kin varied. Some females had no adult female kin in their groups, while others had as many as seven. BROADER IMPACTS The proposed study will provide a comprehensive model of infant development and empirical data that can be used to better understand human developmental trajectories. Although the maternal environment clearly influences infant phenotype, the role of the mother has been neglected in studies of human evolution. This study will use innovative, noninvasive techniques to provide detailed and systematic data to address these gaps in knowledge. I will also collect paired mother-infant fecal samples for stable isotope analysis to directly monitor weaning. I plan to analyze these paired fecal samples after my dissertation work is completed. The fieldwork portion of my project provides educational and research opportunities for recent college graduates, people from the local community, and undergraduate students. I currently mentor three female research assistants who collect data for my project and the CABS project. I also train project employees from the local community to collect fecal samples and to use hand-held electronic devices to record behavior. When I am in the United States, I supervise Arizona State University undergraduate students in research projects through an undergraduate apprenticeship program. RESEARCH SCHEDULE I am collecting data in Kenya from October 2016 through December 2017. In January 2018, I will begin to conduct laboratory and data analyses and writeup results for publication. Funding from the Leakey Foundation is sought to cover the costs of processing the fecal hormone samples in the Core Assay Facility directed by Dr. Jacinta Beehner at the University of Michigan from January 2018 June 2018. DATA SHARING The results of this project will be presented at professional conferences and published in peer-reviewed journals. Data will be shared with project collaborators and members of the Comparative Analysis of Baboon Sociality Project, directed by Dr. Joan Silk.
|Effective start/end date||4/1/17 → 3/31/18|
- Leakey (Louis S. B.) Foundation: $15,000.00
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