The evolution of ecological flexibility, large brains, and long lives: capuchin monkey genomics revealed with fecalFACS

ABSTRACT Ecological flexibility, extended lifespans, and large brains, have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have the largest relative brain size of any monkey and a lifespan that exceeds 50 years, despite their small (3-5 kg) body size. We assemble a de novo reference genome for Cebus imitator and provide the first genome annotation of a capuchin monkey. Through high-depth sequencing of DNA derived from blood, various tissues and feces via fluorescence activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of non-invasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides new insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity. SIGNIFICANCE Surviving challenging environments, living long lives, and engaging in complex cognitive processes are hallmark characteristics of human evolution. Similar traits have evolved in parallel in capuchin monkeys, but their genetic underpinnings remain unexplored. We developed and annotated a reference assembly for white-faced capuchin monkeys to explore the evolution of these phenotypes. By comparing populations of capuchins inhabiting rainforest versus dry forests with seasonal droughts, we detected selection in genes associated with kidney function, muscular wasting, and metabolism, suggesting adaptation to periodic resource scarcity. When comparing capuchins to other mammals, we identified evidence of selection in multiple genes implicated in longevity and brain development. Our research was facilitated by our new method to generate high- and low-coverage genomes from non-invasive biomaterials.