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Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat
Mammalian olfactory receptors (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoires is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of more specialized OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed leaf-nosed bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous versus duplicated receptors among Carollia species, and identified orthologous receptors and associated paralogs to explore the diversity and redundancy of the receptor gene repertoire. The most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two more generalist species (sowelli, perspicillata), but we discovered a few unique sets of ORs within C. castanea with exceptional redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants to an extent that the other species cannot. C. perspicillata, the species with the most generalist diet, had a larger diversity of functional receptors, suggesting the ability to detect a wider range of odorant molecules. The variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication plays a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants.
Species tree disequilibrium positively misleads models of gene family evolution
Gene duplication is a key source of evolutionary innovation, and multigene families evolve in a birth-death process, continuously duplicating and pseudogenizing through time. To empirically test hypotheses about adaptive expansion and contraction of multigene families across species, models infer gene gain and loss in light of speciation events and these inferred gene family expansions may lead to interpretations of adaptations in particular lineages. While the relative abundance of a gene subfamily in the subgenome may reflect its functional importance, tests based on this expectation can be confounded by the complex relationship between the birth-death process of gene subfamily evolution and the species phylogeny. Using simulations, we confirmed tree heterogeneity as a confounding factor in inferring multi-gene adaptation, causing spurious associations between shifts in birth-death rate and lineages with higher branching rates. We then used the olfactory receptor (OR) repertoire, the largest gene family in the mammalian genome, of different bat species with divergent diets to test whether expansions in olfactory receptors are associated with shifts to frugivorous diets. After accounting for tree heterogeneity, we robustly inferred that certain OR subfamilies exhibited expansions associated with dietary shifts to frugivory. Taken together, these results suggest ecological correlates of individual OR gene subfamilies can be identified, setting the stage for detailed inquiry into within-subfamily functional differences.