Selection and local adaptation in capuchin monkeys revealed through fluorescence-activated cell sorting of feces (fecalFACS)

Background: Capuchins have the largest relative brain size of any monkey and a remarkable lifespan of 55 years, despite their small body size. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence, dietary diversity, and ecological flexibility. Despite decades of research into their ecology and life history, little is known about the genomics of this radiation. Results: We assemble a de novo reference genome for Cebus imitator, and provide the first genome annotation of a capuchin monkey. We identified 20,740 and 9,556 for protein-coding and non-coding genes, and recovered 23,402 orthologous groups. Through a comparative genomics approach across a diversity of mammals, we identified genes under positive selection associated with longevity and brain development, which are of particular relevance to capuchin and primate comparative biology. Additionally, we compared populations in distinct habitats, facilitated by our novel method for minimally-biased, whole-genome sequencing from fecal DNA using fluorescence activated cell sorting (FACS). By analyzing 23 capuchin genomes from tropical dry forest and rainforest, we identified population divergence in genes involved in water balance, kidney function, and metabolism, consistent with local adaptation to resource seasonality. Conclusions: Our comparative study of capuchin genomics provides new insights into the molecular basis of brain evolution and longevity. These data also improve our understanding of processes of local adaptation to diverse and physiologically challenging environments. Additionally, we provide a technological advancement in use of non-invasive genomics to study free-ranging mammals through FACS.