RESEARCH

- Overview -

The major focus of my research program is on the comparative socioecology and mating systems of primates, particularly primates of the neotropics.  Specifically, I conduct long-term behavioral and ecological field research on several species in the primate community of Amazonian Ecuador to investigate the ways in which ecological conditions (such as the abundance and distribution of food resources) and the strategies of conspecifics together shape primate behavior and social relationships and ultimately determine the kinds of societies we see primates living in.  This is a crucial and central focus in evolutionary anthropology, as understanding the ways in which behavior and social systems are shaped by environmental pressures is a fundamental part of the discipline.  Additionally, I complement my field studies with molecular genetic laboratory work in order to address issues that are typically difficult to explore through observational studies alone, including questions about dispersal behavior, gene flow, mating patterns, population structure, and the fitness consequences of individual behavior.  In collaboration with colleagues, I have also started using molecular techniques to investigate a number of broader questions concerning the evolutionary history, social systems, and ecological roles of various New World primates.

- Field Work -

I am, first and foremost, a field primatologist, and I either am directly involved in or supervise a very diverse array of field studies on New World primates.  The major portion of my field research takes place at two different sites in the Yasuní Biosphere Reserve in Amazonian Ecuador – at the Proyecto Primates Research Area, which I established in 1994 as a Ph.D. student with Dr. Peter Rodman (UC Davis), and at the Tiputini Biodiversity Station, located approximately 40 km away.  Both of these sites are home to a diverse primate community consisting of 10 to 12 different species.  Additionally, I collaborate on a number of projects involving fieldwork in other New World sites outside of Ecuador. Some of my ongoing field projects are described in more detail below.

Behavior and Ecology of Ateline Primates

Ateline primates – howler monkeys, woolly monkeys, spider monkeys, and muriquis – are a closely related group of New World monkeys that shared a common ancestor roughly 16 million years ago and that, today, manifest marked differences in foraging strategies and patterns of social organization, making them an excellent natural system for comparative study.  Interestingly, however, all members of this clade of primates are characterized by a tendency for females to disperse from their natal social groups prior to reproduction and for some degree of male philopatry, which are both features of social organization that they share with the African great apes.

Prompted by this convergence with African hominoids (and, presumably, with our earliest human ancestors), much of my field research to date has centered on ateline primates.  In my doctoral research and in follow-up work as a postdoctoral fellow, I focused on documenting the natural history, time allocation patterns, ranging behavior, diet, and foraging strategies of lowland woolly monkeys (Lagothrix poeppigii), particularly as they relate to conditions of changing resource abundance.  The results of some of this work – including the unexpected significance of animal prey foraging for this otherwise largely frugivorous primate – are outlined in my publications on the ecological strategies and ranging behavior of woolly monkeys.

My more recent field work on atelines has focused on woolly monkey social behavior and population genetic structure and on comparing the social behavior, foraging strategies, seed dispersal behavior, and cognitive ecology of woolly monkeys with those of sympatric white-bellied spider monkeys (Ateles belzebuth) a closely-related primate that differs markedly in social organization.  These various field projects, conducted in collaboration with several of my current graduate students, form the basis for a number of recent publications and presentations at professional meetings.

Evolution of Monogamy and Pair-Bonding in Primates

A second area of my ongoing fieldwork concerns several other members of the Yasuní primate community.  Since 2002, I have been conducting a long-term study of the evolution of “monogamous” or "pair-bonded" social systems in primates using three species of New World monkeys – owl monkeys, titi monkeys, and sakis – as models.  This work represents an international collaboration with Dr. Eduardo Fernandez-Duque (Fundación ECO, Argentina and CRES (Conservation and Research for Endangered Species), Zoological Society of San Diego), who studies one of these taxa (owl monkeys) at his field site in Argentina.

Monogamy is a rare social system in mammals, and the specific pressures leading to its evolution are still debated.  Early hypotheses forwarded to explain the evolution of monogamy tended to fall into one of two classes.  Some proposed that monogamy evolved in response to the need for biparental care in order to successfully rear offspring, while others envisioned monogamy as the default social system imposed upon males in cases where the dispersion of females makes it difficult for single males to successfully defend access to more than one.  More recently, emphasis has turned to the role of direct mate guarding of individual females by males and to the importance of specific male-female bonds as an infanticide-prevention strategy, with "monogamy" then emerging as a tradeoff between the competing reproductive strategies of males and females. In this project, we are trying to evaluate these various hypotheses for the origin and maintenance of monogamy in primates using a comparative approach, collecting comparable behavioral, ecological, demographic, and genetic data on all three genera at my study site in Ecuador and on one of the taxa (owl monkeys) at study sites in both Ecuador and Argentina. As an additional component of this project, I am currently working in the laboratory to develop novel molecular genetic markers to allow paternity and population structure analyses for these monogamous species.

Investigations of New World Monkey Social Systems

Since my postdoctoral training in the Molecular Genetics Laboratory at the National Zoological Park, Smithsonian Institution, I have been using molecular genetic techniques to complement my field studies and, specifically, to study the dispersal patterns, mating systems, and population structure of several New World primates, including woolly monkeys, spider monkeys, howler monkeys, and golden lion tamarins.  Although each of these taxa has been the subject of long-term observational studies in the wild, data concerning their mating systems and dispersal patterns remain quite limited, which is what initially prompted me to tackle these topics using genetic techniques.  When I began my molecular studies, few variable molecular markers had been identified for New World monkeys.  Thus, an important part of my laboratory work over the past six years has been the isolation and identification of suitable markers for population studies of New World monkeys.  As part of my postdoctoral work and my early laboratory work at NYU, I isolated a large set of variable microsatellite markers for woolly monkey and subsequently screened those for variation in other New World primates, finding many of them to be variable across multiple platyrrhine genera.

Using these markers to genotype woolly monkeys from my study populations, I found that males within some social groups appear to be more closely related to one another than are females.  This pattern is consistent with what we would expect if females were the dispersing sex and males the more philopatric one, as was predicted based on observations of other atelines and in contrast to the pattern seen among most mammals.  However, my results also revealed evidence of significant male gene flow in addition to dispersal by females, a somewhat unexpected finding and one with implications for understanding patterns of social behavior within woolly monkey troops.

I am now using these and additional loci to genotype samples collected from the spider monkey community at my field site.  This population has been under nearly-continuous study since 1994, with all of the animals being individually known and recognized, and my students and collaborators have amassed a large set of behavior data about individuals in the community.  With the genotype data, I will be able to evaluate the dispersal pattern for this population (e.g., is dispersal female-biased or male-biased or do both sexes disperse at roughly equal frequency) and well as test whether patterns of affiliative behavior within the community are concordant with genetic relatedness, as would be predicted by kin selection theory.

Initial analysis of a large set of samples collected from two social groups of spider monkeys during my 2003 to 2005 field seasons reveal results similar to that seen in woolly monkeys – in one group, males are, on average, much more closely-related to one another than are females, consistent with our impression of them as a male-philopatric taxon, while in a second group, there is no difference between the sexes in average pairwise relatedness.  I have also conducted preliminary parentage analyses for offspring born in these two groups and found that, as suggested by field observations of polygamous mating by females, paternity for the current set of offspring is shared among several of the males within each group.

Another major molecular project I am currently involved in is a collaborative study that I began as a postdoctoral researcher with Dr. Jim Dietz (University of Maryland) and Dr. Andy Baker (Philadelphia Zoo).  We are investigating genetic diversity, paternity, and incest avoidance in a wild population of golden lion tamarins (Leontopithecus rosalia), which are highly endangered primates endemic to the Atlantic coastal forests of Brazil. 

Over the last year, I have identified a set of 19 microsatellite loci that are variable in golden lion tamarins by screening a large set of loci isolated from other primates.  I am currently working on genotyping close to 200 individuals from ~20 social groups sampled by my collaborators over the past two decades.  Using these genotype data, we aim to examine, for the first time in a large, wild primate population, the extent to which paternity is shared among males in polyandrous groups (and whether the pattern of paternity-sharing matches predictions from reproductive skew theory) as well as to assess the level of extragroup paternity.  More interestingly from a conservation perspective, we will be able to evaluate whether genetic diversity continues to be lost in this isolated population by comparing diversity estimates at different points in the population’s history, a study that could have important implications for wildlife management.

Finally, since I am one of only a few researchers working on population genetics of New World primates, I have also participated in several other collaborations.  For example, I have worked with Dr. Rudy Rudran (National Zoological Park, Smithsonian Institution) assessing the genetic variation within a population of red howler monkeys in the llanos of Venezuela, and, more recently, conducted preliminary work on the population genetics of muriquis (Brachyteles arachnoides) – another critically endangered primate from Brazil – in collaboration with Dr. Karen Strier (University of Michigan) and Dr. Valéria Fagundes (Universidade Federal do Espírito Santo, Brazil).  In the coming years, I hope to expand that collaboration to examine patterns of paternity in the wild muriqui groups that are the focus of Dr. Strier's research.

New World Monkey Phylogenetics

Through a collaboration with my current colleague, Dr. Todd Disotell, and his postdoctoral associate, Dr. Anthony Tosi, I am also beginning to address questions concerning the phylogeny and evolutionary history of New World primates.  Molecular studies of New World monkeys have lagged far behind those of Old World primates, and the phylogenetic relationships among several major groups of platyrrhine primates remain unresolved.  For example, the branching order of the three major radiations of New World primates – the atelines (Family Atelidae), the sakis and uakaris (Family Pitheciidae), and the cebines and callitrichines (Family Cebidae) is still subject to debate, as are the relationships among the various ateline genera and the genus-level relationships within the Cebidae.  We have made some progress in examining the higher-order phylogeny of the New World monkeys by sequencing several nuclear loci (one autosomal and one each from the X and Y chromosomes) from select genera from each of the currently recognized platyrrhine subfamilies with the aim of trying to nail down these relationships.  Additionally, in just the past few months, I have begun looking at whether generic-level relationships within the Cebidae and Atelidae might be further resolved using Alu elements, building on recently published work by other researchers.  These phylogenetic studies will provide the foundation for developing a database of DNA sequence data for New World monkeys that we plan to establish over the next few years.

Methodological Contributions

In the course of my genetic work, I have been involved in the development and application of several methodological innovations with broader impact for molecular ecological studies of primates.  As a postdoctoral researcher, for example, I helped to develop a now widely-used "subtractive hybridization enrichment" methodology that facilitates the isolation of new microsatellite loci from a taxon.  In addition, in my fieldwork on atelines I perfected the use of inexpensive, home-made biopsy darts for collecting tissue samples from arboreal primates, obviating many of the risks associated with tranquilizing and recovering canopy-dwelling subjects.  Most recently, I developed a rapid and simple PCR-based test for determining the sex of a primate DNA sample that should be of use to many primatologists.  While several molecular methods had already been developed for sex assignment in humans, very few had proven useful in other primates.  By contrast, my sex-typing assay is applicable to taxa from across the primate order and can be effectively used on even the small amounts of DNA recovered from noninvasively collected samples such as hair or feces.

- Additional Research Interests -

Beyond my work on the behavior, ecology, and genetics of New World primates, I have a number of additional academic interests that I continue to pursue with various degrees of formality.  First, I continue to collaborate with another graduate school colleague, Dr. Drew Rendall, on more theoretical issues concerning the evolution of primate social organization and behavior.  With Dr. Rendall, I have co-authored several papers documenting the importance of phylogeny as a constraint on primate social evolution, outlining how phylogenetic methods may be used in studying the evolution of behavior, and defending the use of behavioral characters, in addition to morphological and molecular ones, in phylogeny reconstruction.  We have recently been invited to extend our work to considering the influence of phylogeny on primate cognition.

Second, I continue to dabble in the fields of computer programming and “simulation modeling” of primate behavior, something I began doing as a graduate student.  To this end, I am currently working with one of my students on a model to examine the landscape pattern of “seed rain” produced by spider monkeys as they swallow, transport, and defecate seeds of the fruits they consume as a tool for exploring the ecological significance of these key seed dispersers in neotropical forests.

Finally, although I do not work directly in this field, I maintain a very strong interest in human behavioral ecology and the interface between that field and current conservation issues in the neotropics.  I am especially interested how the subsistence ecology of traditional human populations is impacted by transitioning subsistence technologies, increased mobility, and easier access to markets where forest products (e.g., bushmeat, timber) can be sold, as these issues have very clear implications for the conservation of many areas of the neotropics.