Fruit odorants mediate co-specialization in a multispecies plant-animal mutualism.

Despite the widespread notion that animal-mediated seed dispersal led to the evolution of fruit traits that attract mutualistic frugivores, the dispersal syndrome hypothesis remains controversial, particularly for complex traits such as fruit scent. Here, we test this hypothesis in a community of mutualistic, ecologically important neotropical bats (Carollia spp.) and plants (Piper spp.) that communicate primarily via chemical signals. We found greater bat consumption is significantly associated with scent chemical diversity and presence of specific compounds, which fit multi-peak selective regime models in Piper. Through behavioural assays, we found Carollia prefer certain compounds, particularly 2-heptanol, which evolved as a unique feature of two Piper species highly consumed by these bats. Thus, we demonstrate that volatile compounds emitted by neotropical Piper fruits evolved in tandem with seed dispersal by scent-oriented Carollia bats. Specifically, fruit scent chemistry in some Piper species fits adaptive evolutionary scenarios consistent with a dispersal syndrome hypothesis. While other abiotic and biotic processes likely shaped the chemical composition of ripe fruit scent in Piper, our results provide some of the first evidence of the effect of bat frugivory on plant chemical diversity.

Functional differences in echolocation call design in an adaptive radiation of bats.

All organisms have specialized systems to sense their environment. Most bat species use echolocation for navigation and foraging, but which and how ecological factors shaped echolocation call diversity remains unclear for the most diverse clades, including the adaptive radiation of neotropical leaf-nosed bats (Phyllostomidae). This is because phyllostomids emit low-intensity echolocation calls and many inhabit dense forests, leading to low representation in acoustic surveys. We present a field-collected, echolocation call dataset spanning 35 species and all phyllostomid dietary guilds. We analyze these data under a phylogenetic framework to test the hypothesis that echolocation call design and parameters are specialized for the acoustic demands of different diets, and investigate the contributions of phylogeny and body size to echolocation call diversity. We further link call parameters to dietary ecology by contrasting minimum detectable prey size estimates (MDPSE) across species. We find phylogeny and body size explain a substantial proportion of echolocation call parameter diversity, but most species can be correctly assigned to taxonomic (61%) or functional (77%) dietary guilds based on call parameters. This suggests a degree of acoustic ecological specialization, albeit with interspecific similarities in call structure. Theoretical MDPSE are greatest for omnivores and smallest for insectivores. Omnivores significantly differ from other dietary guilds in MDPSE when phylogeny is not considered, but there are no differences among taxonomic dietary guilds within a phylogenetic context. Similarly, predators of non-mobile/non-evasive prey and predators of mobile/evasive prey differ in estimated MDPSE when phylogeny is not considered. Phyllostomid echolocation call structure may be primarily specialized for overcoming acoustic challenges of foraging in dense habitats, and then secondarily specialized for the detection of food items according to functional dietary guilds. Our results give insight into the possible ecological mechanisms shaping the diversity of sensory systems, and their reciprocal influence on resource use.

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat.

Mammalian olfactory receptor genes (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 repertoire diversity 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 specialized, less diverse OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous vs duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli and C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. 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 and changes in OR diversity may play a role in dietary adaptations and underlie ecological interactions between bats and plants.