Lineage-specific histories rather than shared drivers shape olfactory evolution in New World monkeys

Abstract

Variation in primate olfactory receptor gene repertoires has been linked to shared ecological and sensory drivers, including diet, diurnality, and colour vision. Yet within anthropoids, each link rests on a single lineage, leaving unclear whether this variation reflects a shared response to these drivers or lineage-specific histories. Here, we combine genomic data from 80 New World monkey species with CT-based olfactory anatomy and ecological data to investigate the evolutionary processes underlying repertoire variation. Ecological and sensory variables explain little of this variation; even routinely trichromatic, leaf-eating howler monkeys have repertoires of unremarkable size. Instead, convergent reductions in repertoire size arose through distinct genomic routes: extensive gene inactivation in titi monkeys and large structural deletions in squirrel monkeys. Owl monkeys, the only anthropoids that reverted to nocturnality, retained rather than expanded a large ancestral repertoire shared with diurnal capuchins, and instead enlarged their olfactory bulb. Repertoire size covaries with olfactory bulb volume across the radiation, but only partially within lineages: squirrel monkeys show the converse, losing receptors without a matching bulb reduction. Thus, olfactory evolution in New World monkeys reflects historical contingency rather than a shared response, with convergent changes in repertoire size and partial decoupling of genomic and anatomical evolution.