Squirrel monkeys, owl monkeys and capuchin monkeys, collectively called the Cebines, are of particular interest to anthropologists and behavioral ecologists because of diverse social organization and activity patterns, a varied capacity for social learning, and (in the case of capuchin monkeys) parallels to apes and humans in tool use, large brain size, and strategic thinking. They are also the most important model Neotropical primates used in biomedical research, and have been key in our understanding of malarial infection, color vision, cocaine addiction, and ovarian function. However, the utility of the Cebines as model systems could be enhanced greatly if we understood the evolutionary relationships among current populations. In fact, to date, there is no well-supported molecular or morphological hypothesis of evolutionary relationships among populations or species within these genera, and so present interpretations of variation in their behavior, physiology, morphology and life history characteristics lack an evolutionary framework. For example, we know some capuchin populations use tools in the wild and others do not, but we do not know enough about capuchin phylogenetics to estimate how many times or how long ago tool use evolved, or what physical or life history characteristics have evolved in tandem with the acquisition of tool use. One important contribution of this project will be to provide an explicit evolutionary framework to orient the increasing number of researchers in their biomedical, behavioral ecology, and conservation biology studies of these taxa. To this end, using a comparative approach, this research project will create the first detailed molecular phylogenies and biogeographic analyses for the Cebines. These genera are widespread and sympatric across much of Latin America. We will sequence DNA from specimens across the entire geographic range, and then use statistical phylogenetic methods to generate robust phylogenetic hypotheses for each genus. We will examine the pattern and distribution of mitochondrial haplotypes to test biogeography hypotheses using a historical and paleogeological framework. Our protocol is 1) to extract, amplify and sequence three mitochondrial genes from Cebine tissues across Latin America; 2) to reconstruct phylogenetic relationships within and across each genus using parsimony, likelihood and Bayesian approaches; 3) to use fossil calibrations to produce a time tree for Cebines, and 4) to conduct biogeographic and comparative analyses within this framework.
This research will resolve long-standing questions in physical anthropology about the phylogenetic relationships of the Neotropical primates. This project will also impact the field of biogeography in both theory and methodology through our use of new laboratory methods for DNA extraction and amplification from degraded tissues. Our optimization of protocols for DNA extraction and amplification from museum tissues can serve the scientific community, by making these types of specimen more accessible and economical for use in scientific inquiry. At least three areas of data analysis in this study are cutting edge and will be of significant influence to both anthropologists and biologists working on phylogenetics and biogeography. These include our use of new Bayesian modeling applications for estimating divergence time; our joint estimation of alignment and phylogeny for sequences containing indels; and our comparison of the efficacy of several new event-based and model-based techniques for inferring biogeographic history. This research will provide international field and laboratory experiences for both undergraduates and undergraduates. It will also enhance molecular lab techniques and data analysis techniques in the international primatology community through strong collaborative research among U.S. and Latin American researchers. An important applied aspect of this research is the development of a rigorous, quantitative assessment tool to measure the distribution of biodiversity of the target taxa across populations, to be used for conservation priority assessment of widely distributed taxa.
Our research provides valuable contributions to primate biogeography, and carries broad implications for primate conservation biology and the evolution of Neotropical mammals in general. We provided the first comprehensive molecular analysis for relationships among capuchin species. We found capuchins contain two well-supported monophyletic clades, the morphologically distinct ‘gracile’ and ‘robust’ groups. Our time-tree analysis estimated a ~6 million year divergence between the two clades, and a subsequent diversification at 2 million years ago within each of the two clades. Our analyses indicate that the present widespread sympatry between the two capuchin types across the Amazon results form a single explosive invasion (about 400,000 years ago) of robust capuchins from the Atlantic Forest into the Amazon, where gracile capuchins had been living in isolation. We proposed that the genus Cebus as currently recognized should be split into two genera to reflect this distinct evolutionary history: Cebus for the gracile forms and Sapajus for the robust forms. This taxonomic revision has now been adopted by the scientific community and is being used to guide conservation descisions. We have also shown Cebus albifrons as currently construed is paraphyletic, and the taxonomy in this group needs major revision. Through this work, the PI is an invited expert in the 2012 workshop to evaluate conservation status of all Brazilian primates for complete revision of the Red List. We also provided the first whole mitochondrial genome tree for squirrel monkeys, with strong support for a sister relationship between Saimiri boliviensis and all other Saimiri, and for the monophyly of Saimiri oerstedii and Saimiri sciureus sciureus. We found that the currently used taxon Saimiri sciureus is paraphyletic, and are currently sequencing a wider geographic set of genetic samples to determine boundaries of various monophyletic groups within Saimiri. We inferred the crown lineages for extant squirrel monkeys diverged around 1.5 million years ago. We produced the first study explaining the role of ecology and behavior in shaping the evolution of the astonishing facial diversity of neotropical primates. We found both social and ecological factors drive the evolution of facial patterns, but in different ways. Facial patterns are more complex in primates that live in smaller groups and in species that are sympatric with more species in their own genus, suggesting that complex patterns may aid in species recognition. Darkness of coloration on certain parts of the face related to longitude and latitude, indicating a role for protection from solar glare. Facial hair was longer in higher latitudes, consistent with the ‘hair rule’. Our analyses gave the first integrated picture of different evolutionary forces working to shape primate facial diversity. This grant promoted teaching, training and learning of 8 graduate students, 11 undergraduates, including 13 women in laboratory work—extracting DNA and running PCRs, prepping samples for sequencing, analyzing results and helping with manuscript preparation. Our labs included a diverse community of student workers including African-American, Latin American and Hawaiian-Pacific Islander students. The labs are set up so post-docs, graduate students and advanced undergraduate actively train new students. The PI has developed and taught an advanced undergraduate course Primate Molecular Ecology and Biogeography, directly related to grant content, and an introductory genetics course for non-science majors, Genetic Concepts for Human Sciences. She has guest-lectured in Society and Genetics, Anthropology, and Ecology and Evolutionary Biology on the research content of the grant and related social and genetic issues. PI and Co-PI Alfaro mentored an African-American female graduate student in her NSF-DIGG proposal; she will present at an international conference in a symposium on Comparative Biogeography of Neotropical Primates, where she will network with key players in this field. We mentored a Latin American female post-doc who has attained a faculty position at a premier US institution. Networking and collaboration with Brazilian scientists was especially strong; the PI guest-edited an issue of American Journal of Primatology, with 10 articles and 38 authors; 6 articles included international collaborations. This issue resulted from a symposium the PI organized at 2010 International Primatological Society (IPS) meetings. The PI has organized both an international symposium (Comparative Biogeography for Neotropical Primates) and an international roundtable (Capuchin Research Community Roundtable: Working Together Towards a Comparative Biology of Cebus and Sapajus) for the upcoming 2012 IPS meetings. The PI has lectured on research results in the US and several Brazilian cities. Research results from this grant have been disseminated widely through press releases and interviews; media includes New York Times, Science, Scientific American, Nature, BBC and the premier Brazilian science magazine, Pesquisa. The PI was directly involved in public outreach for genetics and societal issues, including UCLA Darwin Evolving speaker series and four public Annual Symposia of the UCLA Institute for Society and Genetics. The PI was master designer and coordinator for a new interdisciplinary major at UCLA: Human Biology and Society—the first class graduated in 2012.
