Evolutionary Genomics of Brazilian Howler Monkeys

Abstract

Genomics of nonhuman primates has expanded, yet most studies consider a single species per genus. Here, we tested for shared and unique evolutionary histories between species within a primate genus to fill this temporal gap. Howler monkeys (genus Alouatta) are the widest-spread neotropical primate radiation. In parts of their range, deforestation and human encroachment threaten these vulnerable species. We assembled 6 de novo long-read reference genomes (n50 ~15Mb), and sequenced 88 howler monkeys (average coverage ~11X) to reconstruct the evolutionary history of four major howler monkey species groups from across Brazil. Genomic population structure contradicts the current IUCN taxonomic classification. We find environmental differences in demography, including an increased proportion of long ROH and decreasing population size estimates in Atlantic Forest howler monkeys, potentially resulting from the increased habitat fragmentation compared to the Amazon rainforest. Finally, we inferred adaptation by comparing signatures of recent positive selection between two howler species using G1 statistics. Results were enriched for genes involved in xenobiotic detoxification, likely related to howlers’ highly folivorous diet, including a new potentially convergent derived nonsynonymous mutation shared with other folivorous colobine monkeys. Notably, only the species that experienced recent outbreaks of yellow fever shows evidence for adaptation at yellow fever virus entry receptors. The identification of shared and unique demographic and adaptive trajectories demonstrates the utility of intragenus comparative genomics to identify the genetic basis of characteristic phenotypes and species-specific conservation concerns.