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 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 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, 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 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 physiologically challenging environments, as well as the molecular basis of brain evolution and longevity.

Positive Selection and Enhancer Evolution Shaped Lifespan and Body Mass in Great Apes

“…Among those genes, we also identified several associated with neurodevelopment and brain functions, implicated with the regulation of memory and emotions, all of which are peculiar great ape features. This finding is consistent with several studies that have proposed a link between increased life span and increased cognitive functions ( Ghirlanda et al 2014 ; Barton and Venditti 2017 ; Orkin et al 2021 ). Since the increase in longevity elicits a greater risk to develop cancer, the rise and fixation of new molecular variants (nonsynonymous substitutions) could have positively contributed to improve the functionality of the immune system and thus be beneficial for the evolution of the most recent primate lineage.…”

“…Similarly, the MLS varies from 13 years in the calabar angwantibo ( Arctocebus calabarensis ) to 55–122 years in great apes (AnAge database: https://genomics.senescence.info/ (accessed 5th November 2021); Tacutu et al 2018 ). Outside great apes, just a few primate species can reach 50 years (e.g., the capuchin monkeys; Muntané et al 2018 ; Orkin et al 2021 ).…”

Positive selection and enhancer evolution shaped lifespan and body mass in great apes

“…Among the genes with positive selections in apes, we identified several associated with diet, metabolism, as well as with the regulation of memory and emotions, all of which are important great ape features. This finding is consistent with several studies that have proposed a link between increased life span and increased cognitive functions (Ghirlanda et al 2014;Barton and Venditti 2017;Orkin et al 2021). Characterizing their molecular evolution could help us to better understand the rise of genetic neurological disorders in humans, such as macrocephaly, cognitive disorders and Parkinson's disease.…”

“…3a-g; Table S1.8-1.9). These genes are involved in important biological functions that characterized the evolution of long-lived species, such as immunity, neurodevelopment, and telomere maintenance (Zhang et al 2013;Gorbunova et al 2014;Orkin et al 2021). For example, PAK1 is an oncogene involved in cytoskeletal reorganization and cortical development (Pan et al 2015).…”

“…Outside great apes, just a few primate species can reach 50 years (e.g. the capuchin monkeys; Muntané et al 2018;Orkin et al 2021).…”