Genomic and phenotypic evidence support visual and olfactory shifts in primate evolution

Sensory trade-offs between vision and olfaction in the evolution and radiation of primates have long been debated. However, insights have been limited by a lack of sensory gene sequences and accompanying functional predictions. Here we conduct large-scale functional analyses of visual and olfactory receptors and related brain regions across extant primates. Our results reveal a visual shift from ultraviolet to violet colour sensitivity in early haplorrhine primates, followed by acceleration in the rhodopsin retinal release rates at the origin of anthropoids, both of which are expected to greatly enhance visual acuity under brighter light conditions. Additionally, we find that the sensitivity of olfactory receptors shifted from narrowly to broadly tuned early in anthropoid evolution. In contrast, strepsirrhines appear to have retained sensitive dim-light vision and underwent functional enhancement of narrowly tuned olfactory receptors. Our models indicate that this would have enhanced odorant discrimination and facilitated olfaction-mediated physiology and behaviour. These differences in tuning patterns of olfactory receptors between major primate lineages mirror well-established morphological differences in external anatomy and brain structures, revealing new mechanisms of olfactory adaptation and evolutionary plasticity. Our multisystem analyses reveal patterns of co-evolution in genomic, molecular and neuroanatomical traits that are consistent with a sensory ‘reallocation’ rather than strict trade-offs. An analysis of genomic, molecular and neuroanatomical traits across extant primates reveals early divergence in visual and olfactory systems of major primate lineages consistent with lineage-specific shifts in diel activity and dietary niche, providing support for a sensory ‘reallocation’ hypothesis.