The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys 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 particu- larly 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 Cen- tral and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator. Through high-depth sequencing of DNA derived from blood, var- ious tissues, and feces via fluorescence-activated cell sorting (fecal- FACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rain- forests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a com- parative genomics approach spanning a wide diversity of mam- mals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologi- cally challenging environments, as well as the molecular basis of brain evolution and longevity.