Convergent Evolutionary Trade-Offs between Olfaction and Vocal Learning in Mammals

Abstract With roles in sourcing food, evading predators, and locating mates, sensory systems have facilitated ecological adaptations in mammalian evolution. While critical to survival, these systems are metabolically demanding, requiring both dedicated sensory organs and specialised brain regions for detection and interpretation of sensory cues. Consequently, the expansion of a given sensory modality is expected to incur energetic costs, requiring reallocation of resources away from other modes of perception. Here we explore whether changes in foraging environments drive a trade-off between olfaction and complex vocal communication in mammals. Specifically, we compare the olfactory receptor (OR) subgenome across 555 species to identify shifts in olfactory repertoires. We correlate these OR counts with foraging categories and brain regions associated with olfaction (olfactory bulb) and vocal learning (cerebellum). We identify negative shifts in quantity and diversity of functional ORs across five lineages, Haplorrhini, Chiroptera, Pinnipedia, Sirenia, and Cetacea, where non-terrestrial foraging and vocal learning have independently evolved. We also find weak but statistically significant associations between foraging strata, olfaction and lateral cerebellar expansion. These results support convergent evolutionary trade-offs between olfaction and vocal communication in mammals, revealing the impact of ecological transitions and energetic constraints on the evolution of mammalian sensory and communication systems.