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While evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness-related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant-visiting from an insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant-visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant-visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants — a potential ecological constraint on sensory evolution. 

Abstract 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. 

Abstract Dietary adaptation is a major feature of phenotypic and ecological diversification, yet the genetic basis of dietary shifts is poorly understood. Among mammals, Neotropical leaf-nosed bats (family Phyllostomidae) show unmatched diversity in diet; from a putative insectivorous ancestor, phyllostomids have radiated to specialize on diverse food sources including blood, nectar, and fruit. To assess whether dietary diversification in this group was accompanied by molecular adaptations for changing metabolic demands, we sequenced 89 transcriptomes across 58 species and combined these with published data to compare ∼13,000 protein coding genes across 66 species. We tested for positive selection on focal lineages, including those inferred to have undergone dietary shifts. Unexpectedly, we found a broad signature of positive selection in the ancestral phyllostomid branch, spanning genes implicated in the metabolism of all major macronutrients, yet few positively selected genes at the inferred switch to plantivory. Branches corresponding to blood- and nectar-based diets showed selection in loci underpinning nitrogenous waste excretion and glycolysis, respectively. Intriguingly, patterns of selection in metabolism genes were mirrored by those in loci implicated in craniofacial remodeling, a trait previously linked to phyllostomid dietary specialization. Finally, we show that the null model of the widely-used branch-site test is likely to be misspecified, with the implication that the test is too conservative and probably under-reports true cases of positive selection. Our findings point to a complex picture of adaptive radiation, in which the evolution of new dietary specializations has been facilitated by early adaptations combined with the generation of new genetic variation. 

Abstract In mammals, social and reproductive behaviors are mediated by chemical cues encoded by hyperdiverse families of receptors expressed in the vomeronasal organ. Between species, the number of intact receptors can vary by orders of magnitude. However, the evolutionary processes behind variation in receptor number, and its link to fitness-related behaviors are not well understood. From vomeronasal transcriptomes, we discovered the first evidence of intact vomeronasal type-1 receptor (V1r) genes in bats, and we tested whether putatively functional bat receptors were orthologous to those of related taxa, or whether bats have evolved novel receptors. Instead of lineage-specific duplications, we found that bat V1rs show high levels of orthology to those of their relatives, and receptors are under comparative levels of purifying selection as non-bats. Despite widespread vomeronasal organ loss in bats, V1r copies have been retained for >65 million years. The highly conserved nature of bat V1rs challenges our current understanding of mammalian V1r function and suggests roles other than conspecific recognition or mating initiation in social behavior. 

Gene duplication is an important process in the evolution of gene content in eukaryotic genomes. Understanding when gene duplicates contribute new molecular functions to genomes through molecular adaptation is one important goal in comparative genomics. In large gene families, however, characterizing adaptation and neofunctionalization across species is challenging, as models have traditionally quantified the timing of duplications without considering underlying gene trees. This protocol combines multiple approaches to detect adaptation in protein duplicates at a phylogenetic scale. We include a description of models for gene tree-species tree reconciliation that enable different types of inference, as well as a practical guide to their use. Although simulation-based approaches successfully detect shifts in the rate of duplica- tion/retention, the conflation between the duplication and retention processes, the distinct trajectories of duplicates under non-, sub-, and neofunctionalization, as well as dosage effects offer hitherto unexplored analytical avenues. We introduce mathematical descriptions of these probabilities and offer a road map to computational implementation whose starting point is parsimony reconciliation. Sequence evolution information based on the ratio of nonsynonymous to synonymous nucleotide substitution rates (dN/dS) can be combined with duplicate survival probabilities to better predict the emergence of new molecular functions in retained duplicates. Together, these methods enable characterization of potentially adaptive candidate duplicates whose neofunctionalization may contribute to phenotypic divergence across species. 

Bats are famous for using their hearing to explore their environments, yet fewer people are aware that these flying mammals have both good night and daylight vision. Some bats can even see in color thanks to two light-sensitive proteins at the back of their eyes: S-opsin which detects blue and ultraviolet light and L-opsin which detects green and red light. Many species of bat, however, are missing one of these proteins and cannot distinguish any colors; in other words, they are completely color-blind. Some bat species found in Central and South America have independently lost their ability to see blue-ultraviolet light and have thus also lost their color vision. These bats have diverse diets – ranging from insects to fruits and even blood – and being able to distinguish color may offer an advantage in many of their activities, including hunting or foraging. The vision genes in these bats, therefore, give scientists an opportunity to explore how a seemingly important trait can be lost at the molecular level. Sadier, Davies et al. now report that S-opsin has been lost more than a dozen times during the evolutionary history of these Central and South American bats. The analysis used samples from 55 species, including animals caught from the wild and specimens from museums. As with other proteins, the instructions encoded in the gene sequence for S opsin need to be copied into a molecule of RNA before they can be translated into protein. As expected, S-opsin was lost several times because of changes in the gene sequence that disrupted the formation of the protein. However, at several points in these bats’ evolutionary history, additional changes have taken place that affected the production of the RNA or the protein, without an obvious change to the gene itself. This finding suggests that other studies that rely purely on DNA to understand evolution may underestimate how often traits may be lost. By capturing ‘evolution in action’, these results also provide a more complete picture of the molecular targets of evolution in a diverse set of bats.