Dietary Diversification and Specialization in Neotropical Bats Facilitated by Early Molecular Evolution.

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.

Foraging shifts and visual preadaptation in ecologically diverse bats.

Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye-expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant-based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and-unusually for echolocating bats-often have large, well-developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar-feeding lineages and the subfamily Stenodermatinae of fig-eating bats fine-tuning pre-existing visual adaptations for specialized purposes.

Andean non-volant small mammals: A dataset of community assemblages of non-volant small mammals from the high Andes.

Information from diversity inventories was used to study patterns of biodiversity and species distribution, to identify potential priority areas for conservation, and to guide future sampling efforts. In this context, we compiled information on non-volant small mammal communities from the high Andes (>2000 m). Here, we present an open source dataset containing information on diversity (species composition, number of individuals captured), inventory design (type of traps, sampling efforts), and environment (habitat) for both unpublished and published information. This study covers 630 mammalian communities, geographically distributed throughout the Andes in Venezuela, Colombia, Ecuador, Peru, Bolivia, Argentina, and Chile. We compiled a total of 26,412 individual records belonging to 240 species; the order with greatest number of records was Rodentia (n = 25,319, 96.06%), followed by Didelphimorphia (n = 373, 1.42%), Eulipotyphla (n = 358, 1.36%) and Paucituberculata, (n = 307, 1.16%). Andean non-volant small mammal communities harbor a range from 1 to 17 species, with 93.06% of sites being composed of one to five species, 27.78% of sites with species richness varying from 6 to 10 species, and 4.17% sites composed of more than 10 species. Multiple sampling methods were used to survey non-volant small mammals; the most representative methods were snap-traps and Sherman traps, or a combination of both, in more than 81% of the studies. This data paper represents the first large dataset of faunal species inventories for the Andes. There are no copyright restrictions associated with the use of this dataset. Please cite this data paper when its data are used total or partially in research or teaching.

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats.

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.

Taxonomic revision of the Andean leaf-eared mouse, Phyllotis andium Thomas 1912 (Rodentia: Cricetidae), with the description of a new species.

The Andean Leaf-eared mouse, Phyllotis andium Thomas 1912, has been considered a widespread medium-size sigmodontine rodent (230 mm of total length and 35 grams approximately) that occurs from Tungurahua, Ecuador, through the Andes, to Lima, Peru. Previous studies performed on Phyllotis noted evidence of morphological geographical variation within the species, which is likely because of the several potential geographical barriers that exist within the distribution range of P. andium. We carried out a taxonomic revision of this species based on qualitative and quantitative morphological analyses of 330 specimens from 92 localities. This included appropriate comparisons with other species of the andium/amicus group and performed molecular analysis based on cytochrome b sequences. As a result, morphologic qualitative analysis suggested the recognition of three different taxa, which are supported by morphologic quantitative and molecular analyses. The three taxa here identified have allopatric distributional ranges separated by important geographic barriers. Following these identification criteria, P. andium is now recognized for the samples from Tungurahua, Ecuador to Huánuco, Peru, and includes melanius and fruticicolus as synonymous; the southern populations from the Ancash and Lima departments, in the western Peruvian Andes, are proposed to represent a new species; and we recognize P. stenops as a valid species with tamborum as a synonym. Finally, we postulate that the diversification of these three species is related to key events in the Andean orogeny.

Descripción del nido de Scolomys melanops (Rodentia, Cricetidae) y su relación con Lepidocaryum tenue (Arecales, Arecaceae)

Se describe el nido de Scolomys melanops (Rodentia: Cricetidae), encontrado en el Nororiente de Perú en un hábitat de Colinas bajas. Se identificó tres estructuras en el nido: a) Orificio de acceso y salida; b) Túnel y c) Dormidero, en este último se encontraron restos de frutos, fibras del pedúnculo y tallos de Lepidocaryum tenue (Arecales: Arecaceae) "Irapay". Se sugiere en base al material vegetal encontrado en el nido, la existencia de una relación de depredación entre el roedor Scolomys melanops y la palmera Lepidocaryum tenue.

We describe the nest of Scolomys melanops, (Rodentia: Cricetidae) found in low hill habitats in northeastern Peru. We identified three structures in the nest: a) an orifice of access and exit; b) a tunnel and c) roosting area. In the last structure, we found fruit and fiber remains of peduncle and stems of Lepidocaryum tenue (Arecales: Arecaceae) "Irapay". Based on the vegetal remains found in the nest, we suggest the existence of a predation relationship between the rodent Scolomys melanops and the palm Lepidocaryum tenue.