New World monkeys (Platyrrhini), a highly diverse primate lineage endemic to Mexico, Central and South America, include howler monkeys (Alouatta spp.), one of the most ecologically successful genera in the region. They have evolved key adaptations including a specialized folivorous diet and distinctive howling calls that carry over long distances in tropical rainforests, conferring critical survival advantages. However, the genetic underpinnings of these adaptations—specifically, the genes involved in fiber digestion, fermentation, and metabolic adaptation for folivory, and those regulating vocalization for howling—remain poorly understood. Elucidating these mechanisms is important for understanding howler monkey adaptive evolution. To elucidate the genetic underpinnings of these adaptive traits, we generate a high-quality genome of the Guyanan red howler monkey (Alouatta macconnelli) through high-fidelity long-read sequencing. Leveraging this assembly, we conduct extensive population genomic analyses to reconstruct the phylogeny and historical introgression events across Alouatta lineages. Furthermore, we systematically identify genetic changes within protein-coding genes and regulatory regions that underlie the adaptive evolution of digestive shifts, changes in energy metabolism, and the enlarged hyoid bone in howler monkeys. Notably, we identify a lineage-specific duplication of FBP1 (fructose-1,6-bisphosphatase 1). Experiments show that subfunctionalized paralogs have lost catalytic activity but retain AMP binding, which reduces AMP-mediated FBPase inhibition, consequently augmenting gluconeogenic capacity. This innovation provides sustained gluconeogenic capacity utilizing short-chain fatty acids from leaf fermentation, securing metabolic homeostasis in howler monkeys. Together, our findings reveal novel mechanisms underlying the adaptive evolution of folivory and howling in howler monkeys, and provide the first genomic reconstruction of their phylogeographic history.
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