My research program focuses on how animals respond behaviorally and physiologically to ecological and environmental adversity, focusing in particular, on two correlated research questions. First, how do mothers optimize reproduction in changing ecological and social conditions? Female reproduction is a highly costly endeavor. While females employ various behavioral and physiological strategies to fuel reproduction, they may also curtail maternal investment when ecological and social conditions are unfavorable. Such maternal divestment may allow mothers to conserve energy for future reproduction, but at a cost to the health and fitness of current offspring. Thus, the second question that drives my research is: how do ecological and social conditions during early life directly or indirectly - through maternal divestment - affect offspring development? Emerging evidence from a number of fields suggest that pre- and postnatal adversity can shape various aspects of offspring development, including growth, the maturation of the immune system, and stress responsivity. The obvious proximate mechanism for these changes is reduced behavioral and energetic investment from mothers, suggesting maternal constraints on development. However, mothers appear to also “program” various aspects of development via hormones and other bioactives that are transmitted via the placenta, during birth, and through nursing, sometimes compensating for maternal nutritional constraints. How these phenotypic adjustments occur, and whether they are adaptive or maladaptive is a key question in research.
To address these questions, I combine long-term studies of fitness and development on wild nonhuman primates to with detailed experimental studies on captive primates to understand causal relationships between ecological and proximate variables on the hand, and developmental responses on the other. To facilitate research on wild populations, I employ an arsenal of noninvasive techniques to examine hormones, inflammatory biomarkers, and gut microbiota from excreta. I also measure stature growth noninvasively with the use of digital photogrammetry and parallel lasers.
Primary Research Projects
1. Physiological Signatures of Variable Weaning Strategies in Wild Geladas.
This is a collaborative project (funded by NSF BCS-1723228 and Leakey Foundation) with Noah Snyder-Mackler (U Washington) and Laurie Reitsema (U Georgia), focusing on the causes and consequences of premature weaning in wild geladas. In humans, extreme cases of premature weaning have been linked to numerous deficits in development, including stunted growth and impaired immunity, yet two aspects of this equation are poor understood: (1) From an evolutionary perspective, what are the conditions that cause early withdrawal of maternal investment? Geladas are a perfect model for this question because extremely stressful social conditions (i.e., alpha male takeovers) that are commonly linked to maternal withdrawal occur frequently in this species. These conditions also allow us to ask: (2) What physiological mechanisms mediate the downstream consequences of premature weaning, specifically in relation to impaired immune development? To address these questions, we are characterizing the trajectory of weaning using isotopic and elemental chemistry and combining this with information on infant growth, a suite of biomarkers of both innate and acquired immunity, and characterization of the infant gut microbiome - a system recently linked to the development of the immune system. We anticipate that these approaches will generate a broader understanding of premature weaning and its consequences in both nonhumans and humans.
2. Maternal programming of the infant gut-brain axis in vervet monkeys.
To complement this research, we are also examining the mechanisms by which maternal stress induces alters offspring phenotype in a captive primate population. This is a collaborative project involving my graduate student, Lauren Petrullo, Noah Snyder Mackler, and the Wake Forest University Primate Center. While prenatal programming of infant outcomes through gestational maternal glucocorticoids is now fairly well-established, there are numerous other pathways by which maternal bioactives can reach the infant to alter development during the pre- and postnatal periods. Here we investigate how experimentally induced prolonged social stress during early gestation and the perinatal period can cause vervet monkey mothers to alter infant development specifically via maternal hormones and gut microbiota that are vertically transmitted to offspring via the placenta, during birth, and through breastmilk. Towards this end, we have (1) validated the measurement of steroid hormones from breastmilk and infant hair, and (2) characterized the milk microbiome of mothers and the gut microbiome of infants. Together, these preparatory steps will allow us to tackle larger questions of maternally-programmed developmental plasticity in somatic growth, immune development, and stress reactivity in this captive vervet population.
To address these questions, I combine long-term studies of fitness and development on wild nonhuman primates to with detailed experimental studies on captive primates to understand causal relationships between ecological and proximate variables on the hand, and developmental responses on the other. To facilitate research on wild populations, I employ an arsenal of noninvasive techniques to examine hormones, inflammatory biomarkers, and gut microbiota from excreta. I also measure stature growth noninvasively with the use of digital photogrammetry and parallel lasers.
Primary Research Projects
1. Physiological Signatures of Variable Weaning Strategies in Wild Geladas.
This is a collaborative project (funded by NSF BCS-1723228 and Leakey Foundation) with Noah Snyder-Mackler (U Washington) and Laurie Reitsema (U Georgia), focusing on the causes and consequences of premature weaning in wild geladas. In humans, extreme cases of premature weaning have been linked to numerous deficits in development, including stunted growth and impaired immunity, yet two aspects of this equation are poor understood: (1) From an evolutionary perspective, what are the conditions that cause early withdrawal of maternal investment? Geladas are a perfect model for this question because extremely stressful social conditions (i.e., alpha male takeovers) that are commonly linked to maternal withdrawal occur frequently in this species. These conditions also allow us to ask: (2) What physiological mechanisms mediate the downstream consequences of premature weaning, specifically in relation to impaired immune development? To address these questions, we are characterizing the trajectory of weaning using isotopic and elemental chemistry and combining this with information on infant growth, a suite of biomarkers of both innate and acquired immunity, and characterization of the infant gut microbiome - a system recently linked to the development of the immune system. We anticipate that these approaches will generate a broader understanding of premature weaning and its consequences in both nonhumans and humans.
2. Maternal programming of the infant gut-brain axis in vervet monkeys.
To complement this research, we are also examining the mechanisms by which maternal stress induces alters offspring phenotype in a captive primate population. This is a collaborative project involving my graduate student, Lauren Petrullo, Noah Snyder Mackler, and the Wake Forest University Primate Center. While prenatal programming of infant outcomes through gestational maternal glucocorticoids is now fairly well-established, there are numerous other pathways by which maternal bioactives can reach the infant to alter development during the pre- and postnatal periods. Here we investigate how experimentally induced prolonged social stress during early gestation and the perinatal period can cause vervet monkey mothers to alter infant development specifically via maternal hormones and gut microbiota that are vertically transmitted to offspring via the placenta, during birth, and through breastmilk. Towards this end, we have (1) validated the measurement of steroid hormones from breastmilk and infant hair, and (2) characterized the milk microbiome of mothers and the gut microbiome of infants. Together, these preparatory steps will allow us to tackle larger questions of maternally-programmed developmental plasticity in somatic growth, immune development, and stress reactivity in this captive vervet population.
