Karyotypic stasis and swarming influenced the evolution of viral tolerance in a species-rich bat radiation.

The emergence of COVID-19 and severe acute respiratory syndrome (SARS) has prioritized understanding bats' viral tolerance. Myotis bats are exceptionally species rich and have evolved viral tolerance. They also exhibit swarming, a cryptic behavior where large, multi-species assemblages gather for mating, which has been hypothesized to promote interspecific hybridization. To resolve the coevolution of genome architecture and their unusual antiviral tolerance, we undertook a phylogenomic analysis of 60 Old World Myotis genomes. We demonstrate an extensive history of introgressive hybridization that has replaced the species phylogeny across 17%-93% of the genome except for pericentromeric regions of macrochromosomes. Introgression tracts were enriched on microchromosome regions containing key antiviral pathway genes overexpressed during viral challenge experiments. Together, these results suggest that the unusual Myotis karyotype may have evolved to selectively position immune-related genes in high recombining genomic regions prone to introgression of divergent alleles, including a diversity of interleukin loci responsible for the release of pro-inflammatory cytokines.

The genome sequence of the Soprano Pipistrelle, Pipistrellus pygmaeus (Leach, 1825).

We present a genome assembly from an individual male Pipistrellus pygmaeus (the Soprano Pipistrelle; Chordata; Mammalia; Chiroptera; Vespertilionidae). The genome sequence is 1,895.1 megabases in span. Most of the assembly is scaffolded into 23 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 17.18 kilobases in length.

Out of Southeast Asia: A new species of thick-thumbed bat (Chiroptera: Vespertilionidae: Glischropus) from Meghalaya, north-eastern India.

Thick-thumbed bats of the genus Glischropus are currently composed of four recognized species from Southeast Asia, two of which were described in recent times. Among these species, G. aquilus is endemic to Sumatra, G. javanus is restricted to western Java, whereas G. bucephalus is widely distributed north to the Isthmus of Kra and G. tylopus is widespread south to this zoogeographic boundary. Two recently collected Glischropus specimens from Meghalaya state in north-eastern India extend the known distribution range of the genus westward into South Asia by ca. 1000 km. Morphological examination of these specimens and comparison with all known species in this genus revealed marked differences in colouration, dental characters and bacular traits. We therefore describe the Meghalaya specimens as a new species. The discovery of the new species from a forest patch adjacent to Nongkhyllem Wildlife Sanctuary from where another specialized bamboo-dwelling species (Eudiscopus denticulus) was reported recently also underscore the importance of the area from a conservation point of view.

Food for everyone: Differential feeding habits of cryptic bat species inferred from DNA metabarcoding.

Ecological theory postulates that niches of co-occurring species must differ along some ecological dimensions in order to allow their stable coexistence. Yet, many biological systems challenge this competitive exclusion principle. Insectivorous bats from the Northern Hemisphere typically form local assemblages of multiple species sharing highly similar functional traits and pertaining to identical feeding guilds. Although their trophic niche can be accessed with unprecedented details using genetic identification of prey, the underlying mechanisms of resource partitioning remain vastly unexplored. Here, we studied the differential diet of three closely-related bat species of the genus Plecotus in sympatry and throughout their entire breeding season using DNA metabarcoding. Even at such a small geographic scale, we identified strong seasonal and spatial variation of their diet composition at both intra- and interspecific levels. Indeed, while the different bats fed on a distinct array of prey during spring, they showed higher trophic niche overlap during summer and fall, when all three species switched their hunting behaviour to feed on few temporarily abundant moths. By recovering 19 ecological traits for over 600 prey species, we further inferred that each bat species used different feeding grounds and hunting techniques, suggesting that niche partitioning was primarily habitat-driven. The two most-closely related bat species exhibited very distinct foraging habitat preferences, while the third, more distantly-related species was more generalist. These results highlight the need of temporally comprehensive samples to fully understand species coexistence, and that valuable information can be derived from the taxonomic identity of prey obtained by metabarcoding approaches.

Citizen science and online data: Opportunities and challenges for snake ecology and action against snakebite.

The secretive behavior and life history of snakes makes studying their biology, distribution, and the epidemiology of venomous snakebite challenging. One of the most useful, most versatile, and easiest to collect types of biological data are photographs, particularly those that are connected with geographic location and date-time metadata. Photos verify occurrence records, provide data on phenotypes and ecology, and are often used to illustrate new species descriptions, field guides and identification keys, as well as in training humans and computer vision algorithms to identify snakes. We scoured eleven online and two offline sources of snake photos in an attempt to collect as many photos of as many snake species as possible, and attempt to explain some of the inter-species variation in photograph quantity among global regions and taxonomic groups, and with regard to medical importance, human population density, and range size. We collected a total of 725,565 photos-between 1 and 48,696 photos of 3098 of the world's 3879 snake species (79.9%), leaving 781 "most wanted" species with no photos (20.1% of all currently-described species as of the December 2020 release of The Reptile Database). We provide a list of most wanted species sortable by family, continent, authority, and medical importance, and encourage snake photographers worldwide to submit photos and associated metadata, particularly of "missing" species, to the most permanent and useful online archives: The Reptile Database, iNaturalist, and HerpMapper.

Citizen science and online data: opportunities and challenges for snake ecology and action against snakebite

The secretive behavior and life history of snakes makes studying their biology, distribution, and the epidemiology of venomous snakebite challenging. One of the most useful, most versatile, and easiest to collect types of biological data are photographs, particularly those that are connected with geographic location and date-time metadata. Photos verify occurrence records, provide data on phenotypes and ecology, and are often used to illustrate new species descriptions, field guides and identification keys, as well as in training humans and computer vision algorithms to identify snakes. We scoured eleven online and two offline sources of snake photos in an attempt to collect as many photos of as many snake species as possible, and attempt to explain some of the inter-species variation in photograph quantity among global regions and taxonomic groups, and with regard to medical importance, human population density, and range size. We collected a total of 725,565 photos—between 1 and 48,696 photos of 3098 of the world's 3879 snake species (79.9%), leaving 781 “most wanted” species with no photos (20.1% of all currently-described species as of the December 2020 release of The Reptile Database). We provide a list of most wanted species sortable by family, continent, authority, and medical importance, and encourage snake photographers worldwide to submit photos and associated metadata, particularly of “missing” species, to the most permanent and useful online archives: The Reptile Database, iNaturalist, and HerpMapper.

Philippine bats of the genus Kerivoula (Chiroptera: Vespertilionidae): Overview and assessment of variation in K. pellucida and K. whiteheadi.

Bats of the genus Kerivoula (Mammalia, Chiroptera) are widespread in the Philippines with four reported species, but have been poorly known due to a paucity of specimens. We provide the first molecular phylogeny for Philippine Kerivoula, which supports the existence of four distinct clades that we treat as species (K. hardwickii, K. papillosa, K. pellucida, and K. whiteheadi); these four overlap broadly geographically. Each of these may be recognized on the basis of cytochrome b sequences and external and craniodental morphology. Detailed examination of K. pellucida shows little geographic differentiation within the Philippines, but they differ subtly from those on the Sunda Shelf. We consider K. whiteheadi to be composed of four recognizable clades, each restricted to a geographic region within the Philippines. We consider K. bicolor, from peninsular Thailand, and K. pusilla, from Borneo, to be distinct from K. whiteheadi. Our data indicate the presence of two species within the Philippines currently lumped as K. hardwickii; further study of these is needed. A calibrated phylogeny suggests that Kerivoula began arriving in the Philippines about 10 MYA, with each of the four current lineages arriving independently.

Diversification rates have no effect on the convergent evolution of foraging strategies in the most speciose genus of bats, Myotis.

Adaptive radiations are defined as rapid diversification with phenotypic innovation led by colonization to new environments. Notably, adaptive radiations can occur in parallel when habitats with similar selective pressures are accessible promoting convergent adaptions. Although convergent evolution appears to be a common process, it is unclear what are the main drivers leading the reappearance of morphologies or ecological roles. We explore this question in Myotis bats, the only Chiropteran genus with a worldwide distribution. Three foraging strategies-gleaning, trawling, and aerial netting-repeatedly evolved in several regions of the world, each linked to characteristic morphologies recognized as ecomorphs. Phylogenomic, morphometric, and comparative approaches were adopted to investigate convergence of such foraging strategies and skull morphology as well as factors that explain diversification rates. Genomic and morphometric data were analyzed from ∼80% extant taxa. Results confirm that the ecomorphs evolved multiple times, with trawling evolving more often and foliage gleaning most recently. Skull morphology does not reflect common ancestry and evolves convergently with foraging strategy. Although diversification rates have been roughly constant across the genus, speciation rates are area-dependent and higher in taxa with temperate distributions. Results suggest that in this species-rich group of bats, first, stochastic processes have led divergence into multiple lineages. Then, natural selection in similar niches has promoted repeated adaptation of phenotypes and foraging strategies. Myotis bats are thus a remarkable case of ecomorphological convergence and an emerging model system for investigating the genomic basis of parallel adaptive radiation.

The menu varies with metabarcoding practices: A case study with the bat Plecotus auritus.

Metabarcoding of feces has revolutionized the knowledge of animal diets by providing unprecedented resolution of consumed resources. However, it is still unclear how different methodological approaches influence the ecological conclusions that can be drawn from such data. Here, we propose a critical evaluation of several data treatments on the inferred diet of the bat Plecotus auritus using guano regularly collected from various colonies throughout the entire active season. First and unlike previous claims, our data indicates that DNA extracted from large amounts of fecal material issued from guano accumulates yield broader taxonomic diversity of prey than smaller numbers of pellets would do, provided that extraction buffer volumes are adapted to such increased amounts of material. Second, trophic niche analyses based on prey occurrence data uncover strong seasonality in the bat's diet and major differences among neighboring maternity colonies. Third, while the removal of rare prey items is not always warranted as it introduces biases affecting particularly samples with greater prey species richness. Fourth, examination of distinct taxonomic depths in diet analyses highlights different aspects of food consumption providing a better understanding of the consumer's diet. Finally, the biologically meaningful patterns recovered with presence-absence approaches are virtually lost when attempting to quantify prey consumed using relative read abundances. Even in an ideal situation where reference barcodes are available for most potential prey species, inferring realistic patterns of prey consumption remains relatively challenging. Although best practice in metabarcoding analyses will depend on the aims of the study, several previous methodological recommendations seem unwarranted for studying such diverse diets as that of brown long-eared bats.

The taxonomic status of Myotis aelleni Baud, 1979 (Chiroptera, Vespertilionidae).

Myotis aelleni Baud, 1979 was described based on a large series from Chubut, Argentina, and is known only from the type locality and Río Negro, also in Argentina. According to the original description, M. aelleni is closest morphologically to M. chiloensis (Waterhouse, 1840), but can be distinguished based on the tricolored dorsal hairs and skull size and shape. The taxonomic status of M. aelleni has been questioned but the species is still treated as valid. Based on qualitative and quantitative analyses of the type series of M. aelleni, and series of M. chiloensis, including the neotype, we recognize M. aelleni as a junior synonym of M. chiloensis. M. aelleni and M. chiloensis have bicolor dorsal hairs and cannot be distinguished on the basis of the skull size and shape. After synonymy, M. chiloensis occur from Central Chile and western Argentina to central Patagonia and Tierra del Fuego archipelago. Twenty-one species of Myotis occur in South America, including Trinidad and Tobago.

A new genus and species of vespertilionid bat from the Indomalayan Region.

Bats belonging to the subfamily Vespertilioninae are diverse and cosmopolitan, but their systematic arrangement remains a challenge. Previous molecular surveys suggested new and unexpected relationships of some members compared to more traditional, morphology-based classifications, and revealed the existence of taxonomically undefined lineages. We describe here a new genus and species corresponding to an enigmatic lineage that was previously identified within the genus Eptesicus in the Indomalayan Region. Phylogenetic reconstructions based on mitochondrial and nuclear genes relate the new taxon to Tylonycteris and Philetor, and show that specimens associated with this new genus represent 2 genetically distinct species. Although little is known about their ecology, locations of capture and wing morphology suggest that members of this new genus are tree-dwelling, open-space aerial insect predators. The new species has only been documented from Yok Don National Park in Vietnam, so its conservation status is uncertain until more surveying methods target the bat fauna of the dipterocarp forest in Southeast Asia.

Porous barriers? Assessment of gene flow within and among sympatric long-eared bat species.

Species are the basic units for measuring biodiversity and for comprehending biological interactions. Yet, their delineation is often contentious, especially in groups that are both diverse and phenotypically conservative. Three cryptic species of long-eared bats, Plecotus auritus, P. austriacus, and P. macrobullaris, co-occur over extensive areas of Western Europe. The latter is a fairly recent discovery, questioning the overall diversity of the entire Plecotus complex. Yet, high morphological and acoustic similarities compromise the reliable identification of long-eared bats in the field. We postulate that such extensive phenotypic overlap, along with the recurrent observation of morphologically intermediate individuals, may hide rampant interspecific hybridization. Based on a geographic sampling centered on areas of sympatry in the Alps and Corsica, we assessed the level of reproductive isolation of these three Plecotus species with mitochondrial and nuclear markers, looking at both inter- and intraspecific genetic population structuring. No sign of hybridization was detected between these three species that appear well separated biologically. Genetic structuring of populations, however, reflected different species-specific responses to environmental connectivity, that is, to the presence of orographic or sea barriers. While the Alpine range and the Ligurian Sea coincided with sharp genetic discontinuities in P. macrobullaris and P. austriacus, the more ubiquitous P. auritus showed no significant population structuration. There were clear phylogeographic discrepancies between microsatellite and mitochondrial markers at the intraspecific level, however, which challenges the reliance on simple barcoding approaches for the delineation of sound conservation units.

Evolution of immune chemoreceptors into sensors of the outside world.

Changes in gene expression patterns represent an essential source of evolutionary innovation. A striking case of neofunctionalization is the acquisition of neuronal specificity by immune formyl peptide receptors (Fprs). In mammals, Fprs are expressed by immune cells, where they detect pathogenic and inflammatory chemical cues. In rodents, these receptors are also expressed by sensory neurons of the vomeronasal organ, an olfactory structure mediating innate avoidance behaviors. Here we show that two gene shuffling events led to two independent acquisitions of neuronal specificity by Fprs. The first event targeted the promoter of a V1R receptor gene. This was followed some 30 million years later by a second genomic accident targeting the promoter of a V2R gene. Finally, we show that expression of a vomeronasal Fpr can reverse back to the immune system under inflammatory conditions via the production of an intergenic transcript linking neuronal and immune Fpr genes. Thus, three hijackings of regulatory elements are sufficient to explain all aspects of the complex expression patterns acquired by a receptor family that switched from sensing pathogens inside the organism to sensing the outside world through the nose.

Comparative phylogeography of African fruit bats (Chiroptera, Pteropodidae) provide new insights into the outbreak of Ebola virus disease in West Africa, 2014-2016.

Both Ebolavirus and Marburgvirus were detected in several fruit bat species of the family Pteropodidae, suggesting that this taxon plays a key role in the life cycle of filoviruses. After four decades of Zaire Ebolavirus (ZEBOV) outbreaks in Central Africa, the virus was detected for the first time in West Africa in 2014. To better understand the role of fruit bats as potential reservoirs and circulating hosts between Central and West Africa, we examine here the phylogeny and comparative phylogeography of Pteropodidae. Our phylogenetic results confirm the existence of four independent lineages of African fruit bats: the genera Eidolon and Rousettus, and the tribes Epomophorini and Scotonycterini, and indicate that the three species suspected to represent ZEBOV reservoir hosts (Epomops franqueti, Hypsignathus monstrosus, and Myonycteris torquata) belong to an African clade that diversified rapidly around 8-7 Mya. To test for phylogeographic structure and for recent gene flow from Central to West Africa, we analysed the nucleotide variation of 675 cytochrome b gene (Cytb) sequences, representing eight fruit bat species collected in 48 geographic localities. Within Epomophorina, our mitochondrial data do not support the monophyly of two genera (Epomops and Epomophorus) and four species (Epomophorus gambianus, Epomops franqueti, Epomops buettikoferi, and Micropteropus pusillus). In Epomops, however, we found two geographic haplogroups corresponding to the Congo Basin and Upper Guinea forests, respectively. By contrast, we found no genetic differentiation between Central and West African populations for all species known to make seasonal movements, Eidolon helvum, E. gambianus, H. monstrosus, M. pusillus, Nanonycteris veldkampii, and Rousettus aegyptiacus. Our results suggest that only three fruit bat species were able to disperse directly ZEBOV from the Congo Basin to Upper Guinea: E. helvum, H. monstrosus, and R. aegyptiacus.

Two Mitochondrial Barcodes for one Biological Species: The Case of European Kuhl's Pipistrelles (Chiroptera).

The Kuhl's pipistrelle (Pipistrellus kuhlii) is a Western Palaearctic species of bat that exhibits several deeply divergent mitochondrial lineages across its range. These lineages could represent cryptic species or merely ancient polymorphism, but no nuclear markers have been studied so far to properly assess the taxonomic status of these lineages. We examined here two lineages occurring in Western Europe, and used both mitochondrial and nuclear markers to measure degrees of genetic isolation between bats carrying them. The sampling focused on an area of strict lineage sympatry in Switzerland but also included bats from further south, in North Africa. All individuals were barcoded for the COI gene to identify their mitochondrial lineages and five highly polymorphic microsatellite loci were used to cluster them according to their nuclear genotypes. Despite this low number of nuclear markers, all North African nuclear genotypes were grouped in a highly distinct subpopulation when compared with European samples sharing the same mitochondrial barcodes. The reverse situation prevailed in Switzerland where bats carrying distinct barcodes had similar nuclear genotypes. There was a weak east/west nuclear structure of populations, but this was independent of mitochondrial lineages as bats carrying either variant were completely admixed. Thus, the divergent mitochondrial barcodes present in Western Europe do not represent cryptic species, but are part of a single biological species. We argue that these distinct barcodes evolved in allopatry and came recently into secondary contact in an area of admixture north of the Alps. Historical records from this area and molecular dating support such a recent bipolar spatial expansion. These results also highlight the need for using appropriate markers before claiming the existence of cryptic species based on highly divergent barcodes.

First record of Myotis albescens (Chiroptera, Vespertilionidae) in French Guiana.

BACKGROUND: Myotis albescens occurs from Mexico southward to Uruguay and Argentina. The species is known for all South American countries except French Guiana and Chile. NEW INFORMATION: Based on one specimen recently collected in French Guiana we fill part of the gap in the distribution of the species in South America. Myotis albescens occurs in the Guiana Shield with other four congeners, from which it can be distinguished by external and skull traits. As an aid to future identifications, we provide a key to this assemblage.

Molecular phylogeny and morphological revision of Myotis bats (Chiroptera: Vespertilionidae) from Taiwan and adjacent China.

In taxonomic accounts, three species of Myotis have been traditionally reported to occur on the island of Taiwan: Watase's bat (M. formosus watasei Kishida), the Formosan broad-muzzled bat (M. muricola latirostris Kishida) and the Formosan mouse-eared bat (M. adversus taiwanensis Linde). The discovery in 1997 of an unknown taxon not fitting to the description of any of these species encouraged us to re-examine more thoroughly the systematics and phylogeny of Myotis bats inhabiting Taiwan. We used a combination of morphologic and molecular methods to aid the identification of the different taxa from this island and reconstruct their phylogenetic relationships. Multivariate analyses based on 17 craniodental characters of 105 specimens caught across Taiwan and further external characters allowed us to discriminate eight taxa of Myotinae co-occurring on this island. A subset of 80 specimens were further sequenced for the cytochrome b gene (1140 bp) and subjected to phylogenetic reconstructions including representative species from adjacent China and from all main lineages of the worldwide Myotis radiation. These molecular reconstructions showed that the Myotinae from Taiwan are phylogenetically diverse and are issued from several independent clades. The genetic results were completely congruent with the phenetic groupings based on craniodental and external morphology, as each of the eight Taiwanese taxa proved to be reciprocally monophyletic. Two unnamed taxa that did not fit into any of the known species were described as species new to science. Furthermore the taxon latirostris usually associated to the Asian M. muricola, was phylogenetically and morphologically distant from any other known Myotis and was assigned here to the fossil (Miocene) genus Submyotodon. Submyotodon latirostris, M. secundus sp. n. and M. soror sp. n. are endemic species from Taiwan, whereas the other five Myotis are more widespread and also found in the mainland. An identification key is provided to ease the discrimination of these Myotinae species in Taiwan and adjacent China.

Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera).

Sequences of the mitochondrial cytochrome b (1140 bp) and nuclear Rag 2 (1148 bp) genes were used to assess the evolutionary history of the cosmopolitan bat genus Myotis, based on a worldwide sampling of over 88 named species plus 7 species with uncertain nomenclature. Phylogenetic reconstructions of this comprehensive taxon sampling show that most radiation of species occurred independently within each biogeographic region. Our molecular study supports an early divergence of species from the New World, where all Nearctic and Neotropical species plus a lineage from the Palaearctic constitute a monophyletic clade, sister to the remaining Old World taxa. The major Old World clade includes all remaining Eurasian taxa, most Oriental species, one Oceanian, and all Ethiopian species. Another lineage, including M. latirostris from Taiwan, appears at the base of these two major biogeographic clades and, because it bears nyctalodont molars, could be considered as a distinct genus. However, this molar configuration is also found in crown-group species, indicating that these dental characters are variable in the genus Myotis and may confound interpretation of the fossil record. Molecular datings suggest an origin of all recent Myotis in the early Miocene (about 21MYA with 95% highest posterior density interval 23-20MYA). This period was characterized by a global climatic cooling that reduced the availability of tropical habitats and favoured the development of more temperate vegetation. This sharp climatic change might have triggered the evolution of Myotis in the Northern continents, because Myotis ancestors seem to have been well adapted and successful in such temperate habitats. Ancestral area reconstructions based on the molecular phylogeny suggest that the eastern portion of the Asian continent was an important center of origin for the early diversification of all Myotis lineages, and involved relatively few subsequent transcontinental range expansions.

Biogeography of Old World emballonurine bats (Chiroptera: Emballonuridae) inferred with mitochondrial and nuclear DNA.

Extant bats of the genus Emballonura have a trans-Indian Ocean distribution, with two endemic species restricted to Madagascar, and eight species occurring in mainland southeast Asia and islands in the western Pacific Ocean. Ancestral Emballonura may have been more widespread on continental areas, but no fossil identified to this genus is known from the Old World. Emballonura belongs to the subfamily Emballonurinae, which occurs in the New and Old World. Relationships of all Old World genera of this subfamily, including Emballonura and members of the genera Coleura from Africa and western Indian Ocean islands and Mosia nigrescens from the western Pacific region, are previously unresolved. Using 1833 bp of nuclear and mitochondrial genes, we reconstructed the phylogenetic history of Old World emballonurine bats. We estimated that these lineages diverged around 30 million years ago into two monophyletic sister groups, one represented by the two taxa of Malagasy Emballonura, Coleura and possibly Mosia, and the other by a radiation of Indo-Pacific Emballonura, hence, rendering the genus Emballonura paraphyletic. The fossil record combined with these phylogenetic relationships suggest at least one long-distance dispersal event across the Indian Ocean, presumably of African origin, giving rise to all Indo-Pacific Emballonura species (and possibly Mosia). Cladogenesis of the extant Malagasy taxa took place during the Quaternary giving rise to two vicariant species, E. atrata in the humid east and E. tiavato in the dry west.

Segmental copy number variation shapes tissue transcriptomes.

Copy number variation (CNV) is a key source of genetic diversity, but a comprehensive understanding of its phenotypic effect is only beginning to emerge. We have generated a CNV map in wild mice and classical inbred strains. Genome-wide expression data from six major organs show not only that expression of genes within CNVs tend to correlate with copy number changes, but also that CNVs influence the expression of genes in their vicinity, an effect that extends up to half a megabase. Genes within CNVs show lower expression and more specific spatial expression patterns than genes mapping elsewhere. Our analyses reveal differential constraint on copy number changes of genes expressed in different tissues. Dosage alterations of brain-expressed genes are less frequent than those of other genes and are buffered by tighter transcriptional regulation. Our study provides initial evidence that CNVs shape tissue transcriptomes on a global scale.