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Frugivory evolved multiple times in mammals, including bats. However, the cellular and molecular components driving it remain largely unknown. Here, we use integrative single-cell sequencing (scRNA-seq and scATAC-seq) on insectivorous (Eptesicus fuscus; big brown bat) and frugivorous (Artibeus jamaicensis; Jamaican fruit bat) bat kidneys and pancreases and identify key cell population, gene expression and regulatory differences associated with the Jamaican fruit bat that also relate to human disease, particularly diabetes. We find a decrease in loop of Henle and an increase in collecting duct cells, and differentially active genes and regulatory elements involved in fluid and electrolyte balance in the Jamaican fruit bat kidney. The Jamaican fruit bat pancreas shows an increase in endocrine and a decrease in exocrine cells, and differences in genes and regulatory elements involved in insulin regulation. We also find that these frugivorous bats share several molecular characteristics with human diabetes. Combined, our work provides insights from a frugivorous mammal that could be leveraged for therapeutic purposes.

Although 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 a presumed 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.

In 1967 G.G. Simpson described three partial mandibles from early Miocene deposits in Kenya that he interpreted as belonging to a new strepsirrhine primate, Propotto. This interpretation was quickly challenged, with the assertion that Propotto was not a primate, but rather a pteropodid fruit bat. The latter interpretation has not been questioned for almost half a century. Here we re-evaluate the affinities of Propotto, drawing upon diverse lines of evidence to establish that this strange mammal is a strepsirrhine primate as originally suggested by Simpson. Moreover, our phylogenetic analyses support the recognition of Propotto, together with late Eocene Plesiopithecus from Egypt, as African stem chiromyiform lemurs that are exclusively related to the extant aye-aye (Daubentonia) from Madagascar. Our results challenge the long-held view that all lemurs are descended from a single ancient colonization of Madagascar, and present an intriguing alternative scenario in which two lemur lineages dispersed from Africa to Madagascar independently, possibly during the later Cenozoic.

Genetic exchange and hybridization appear common among the western long-eared bats from North America. Multiple sources of evidence indicate that lineages within this group are evolving independently, despite genetic exchange. However, evidence of gene flow raises questions about the species-level status of some lineages. C.L. Lausen et al. (2019. Can. J. Zool. 97(3): 267-279) proposed that Myotis evotis (H. Allen, 1864) (long-eared myotis) and Myotis keenii (Merriam, 1895) (Keen's myotis) are one species, not two. This conclusion is based on analyses of cytochrome b and microsatellite data suggesting gene flow between these taxa. Microsatellites are not reliable markers for identifying species because homoplasy can be a major confounding factor, which appears to be true in this case. We reanalyzed the dataset of C.L. Lausen et al. (2019) and show that it is not reliable to distinguish between gene flow or homoplasy, and that these data do not support the conclusion that M. evotis and M. keenii represent a single species. Previous morphological and genomic studies indicate that these are separate species despite previous genetic exchange between them. Failing to recognize that gene flow can occur between independently evolving lineages is counterproductive for conservation because it can lead to neglect of important independent lineages, and likewise failing to use proper tools to delimit species is counterproductive to efforts to quantify biodiversity and design conservation strategies. Key words: bats, species, Myotis evotis, long-eared myotis, Myotis keenii, Keen's myotis, conservation, taxonomy, microsatellites. L'echange genetique et l'hybridation semblent repandus chez les vespertilions a longues oreilles de l'ouest de l'Amerique du Nord. De multiples elements de preuve indiquent que des lignees au sein de ce groupe evoluent de maniere independante, malgre la presence d'echanges genetiques. Des indices d'un flux genetique soulevent toutefois des questions quant au statut d'espece de certaines lignees. C.L. Lausen et al. (2019. Can. J. Zool. 97(3): 267-279) proposent que Myotis evotis (H. Allen, 1864) (vespertilion a longues oreilles) et Myotis keenii (Merriam, 1895) (vespertilion de Keen) representent une seule espece, et non deux. Cette conclusion repose sur des analyses du cytochrome b et de donnees de microsatellites qui indiqueraient un flux genetique entre ces deux taxons. Les microsatellites ne sont pas des marqueurs fiables pour l'identification d'especes puisque l'homoplasie peut constituer un important facteur de confusion, ce qui semble etre le cas dans le present exemple. Nous avons reanalyse l'ensemble de donnees de C.L. Lausen et al. (2019) et demontrons qu'il ne peut pas servir a distinguer de maniere fiable le flux genetique de l'homoplasie et que ces donnees n'appuient pas la conclusion que M. evotis et M. keenii representent une seule et meme espece. Des etudes morphologiques et genomiques passees indiquent qu'il s'agit d'especes distinctes, malgre des echanges genetiques passes entre elles. Le defaut de reconnaitre qu'un flux genetique peut se produire entre des lignees qui evoluent de maniere independante est contreproductif sur le plan de la conservation parce que d'importantes lignees independantes peuvent ainsi ne pas etre prises en consideration, et le fait de ne pas utiliser les bons outils pour delimiter des especes est egalement contreproductif pour ce qui est de quantifier la biodiversite et de concevoir de strategies de conservation. [Traduit par la Redaction] Mots-cles : chauves-souris, especes, Myotis evotis, vespertilion a longues oreilles, Myotis keenii, vespertilion de Keen, conservation, taxonomie, microsatellites., Introduction Bats are one of the most diverse orders of mammals with more than 1400 living species (Simmons and Cirranello 2019). But how are these species delimited? Species delimitation is [...]

Convergence offers an opportunity to explore to what extent evolution can be predictable when genomic composition and environmental triggers are similar. Here, we present an emergent model system to study convergent evolution in nature in a mammalian group, the bat genus Myotis. Three foraging strategies—gleaning, trawling, and aerial hawking, each characterized by different sets of phenotypic features—have evolved independently multiple times in different biogeographic regions in isolation for millions of years. To investigate the genomic basis of convergence and explore the functional genomic changes linked to ecomorphological convergence, we sequenced and annotated 17 new genomes and screened 16,426 genes for positive selection and associations between relative evolutionary rates and foraging strategies across 30 bat species representing all Myotis ecomorphs across geographic regions as well as among sister groups. We identify genomic changes that describe both phylogenetic and ecomorphological trends. We infer that colonization of new environments may have first required changes in genes linked to hearing sensory perception, followed by changes linked to fecundity and development, metabolism of carbohydrates, and heme degradation. These changes may be linked to prey acquisition and digestion and match phylogenetic trends. Our findings also suggest that the repeated evolution of ecomorphs does not always involve changes in the same genes but rather in genes with the same molecular functions such as developmental and cellular processes. [ABSTRACT FROM AUTHOR]

Delimiting species and quantifying their underlying variation is imperative for documenting diversity in highly speciose regions like the Neotropics. To aid with proper delimitation and avoid the perils of inflating or underestimating taxonomic units, approaches combining environmental, genetic, and phenotypic data are essential to provide a holistic perspective based on integrative taxonomy. A multiple-evidence approach is particularly useful when dealing with cryptic or iconic (i.e., easy to identify) species that might contain hidden diversity. We studied the phylogeography of one such species, the frog-eating bat (Trachops), and examined species limits throughout its broad range in the Neotropics. Following previous studies, we tested the hypotheses that Trachops is a monotypic genus with high intraspecific genetic and phenotypic diversity. Multilocus phylogenetics and species-delimitation analyses showed that Trachops consists of at least three species that diverged between seven to three million years ago. Taxonomic limits of three species-level groups recognized in our study (T. cirrhosus, T. coffini, and T. ehrhardti) are confirmed by a cranial morphometric analysis of over 800 individuals and craniodental features. Ecological niche models revealed that each of these groups occupies a dis-tinct niche, and heterogeneous environmental gradients and biogeographic barriers could be responsible for maintaining the limits of these taxa. This study sheds new light into the taxonomy of Trachops that can be important for conservation management in Neotropical areas with a fast rate of deforestation. [ABSTRACT FROM AUTHOR]