Publications by authors named "Emma C Teeling"

66 Publications

Decoding bat immunity: the need for a coordinated research approach.

Nat Rev Immunol 2021 Mar 1. Epub 2021 Mar 1.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

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http://dx.doi.org/10.1038/s41577-021-00523-0DOI Listing
March 2021

Timescale and colony-dependent relationships between environmental conditions and plasma oxidative markers in a long-lived bat species.

Conserv Physiol 2020 14;8(1):coaa083. Epub 2020 Sep 14.

Zoological Institute & Museum, University of Greifswald, Loitzer Str. 26, 17489 Greifswald, Germany.

To increase the applicability and success of physiological approaches in conservation plans, conservation physiology should be based on ecologically relevant relationships between physiological markers and environmental variation that can only be obtained from wild populations. Given their integrative and multifaceted aspects, markers of oxidative status have recently been considered in conservation physiology, but still need to be validated across environmental conditions and locations. Here, we examined whether inter-annual variation in two oxidative markers, plasma antioxidant capacity and plasma hydroperoxides, followed inter-annual variation in temperature anomalies and associated vegetation changes in four colonies of long-lived greater mouse-eared bats () monitored over five consecutive years. We found that the plasma antioxidant capacity of bats decreased while plasma hydroperoxide concentrations increased with increasing temperature anomalies occurring in the two weeks before blood sampling. Moreover, the antioxidant defences of these bats reflected vegetation indices, which themselves reflected the thermal conditions experienced by bats in their foraging habitat. Variation in oxidative markers therefore appears to be due to variation in thermoregulatory costs and to indirect changes in foraging costs. Overall, these results validate the use of markers of oxidative status in conservation physiology to monitor thermal perturbations recently experienced by animals in their natural habitat. However, even though oxidative markers varied in the same direction in all four bat colonies across years, the amplitude of their response differed. If these different physiological responses reflect different performances (e.g. productivity, survival rate) between colonies, this implies that, if necessary, conservation measures may need to be applied at the local scale.
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http://dx.doi.org/10.1093/conphys/coaa083DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7605240PMC
September 2020

Wing: A suitable nonlethal tissue type for repeatable and rapid telomere length estimates in bats.

Mol Ecol Resour 2021 Feb 2;21(2):421-432. Epub 2020 Nov 2.

School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin, Ireland.

Telomeres are used increasingly in ecology and evolution as biomarkers for ageing and environmental stress, and are typically measured from DNA extracted from nonlethally sampled blood. However, obtaining blood is not always possible in field conditions and only limited amounts can be taken from small mammals, such as bats, which moreover lack nucleated red blood cells and hence yield relatively low amounts of DNA. As telomere length can vary within species according to age and tissue, it is important to determine which tissues serve best as a representation of the organism as a whole. Here, we investigated whether wing tissue biopsies, a rapid and relatively noninvasive tissue collection method, could serve as a proxy for other tissues when measuring relative telomere length (rTL) in the Egyptian fruit bat (Rousettus aegyptiacus). Telomeres were measured from blood, brain, heart, kidney, liver lung, muscle and wing, and multiple wing biopsies were taken from the same individuals to determine intra-individual repeatability of rTL measured by using qPCR. Wing rTL correlated with rTL estimates from most tissues apart from blood. Blood rTL was not significantly correlated with rTL from any other tissue. Blood and muscle rTLs were significantly longer compared with other tissues, while lung displayed the shortest rTLs. Individual repeatability of rTL measures from wing tissue was high (>70%). Here we show the relationships between tissue telomere dynamics for the first time in a bat, and our results provide support for the use of wing tissue for rTL measurements.
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http://dx.doi.org/10.1111/1755-0998.13276DOI Listing
February 2021

Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates.

Proc Natl Acad Sci U S A 2020 09 21;117(36):22311-22322. Epub 2020 Aug 21.

The Genome Center, University of California, Davis, CA 95616;

The novel coronavirus severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the cause of COVID-19. The main receptor of SARS-CoV-2, angiotensin I converting enzyme 2 (ACE2), is now undergoing extensive scrutiny to understand the routes of transmission and sensitivity in different species. Here, we utilized a unique dataset of ACE2 sequences from 410 vertebrate species, including 252 mammals, to study the conservation of ACE2 and its potential to be used as a receptor by SARS-CoV-2. We designed a five-category binding score based on the conservation properties of 25 amino acids important for the binding between ACE2 and the SARS-CoV-2 spike protein. Only mammals fell into the medium to very high categories and only catarrhine primates into the very high category, suggesting that they are at high risk for SARS-CoV-2 infection. We employed a protein structural analysis to qualitatively assess whether amino acid changes at variable residues would be likely to disrupt ACE2/SARS-CoV-2 spike protein binding and found the number of predicted unfavorable changes significantly correlated with the binding score. Extending this analysis to human population data, we found only rare (frequency <0.001) variants in 10/25 binding sites. In addition, we found significant signals of selection and accelerated evolution in the ACE2 coding sequence across all mammals, and specific to the bat lineage. Our results, if confirmed by additional experimental data, may lead to the identification of intermediate host species for SARS-CoV-2, guide the selection of animal models of COVID-19, and assist the conservation of animals both in native habitats and in human care.
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http://dx.doi.org/10.1073/pnas.2010146117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7486773PMC
September 2020

Six reference-quality genomes reveal evolution of bat adaptations.

Nature 2020 07 22;583(7817):578-584. Epub 2020 Jul 22.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

Bats possess extraordinary adaptations, including flight, echolocation, extreme longevity and unique immunity. High-quality genomes are crucial for understanding the molecular basis and evolution of these traits. Here we incorporated long-read sequencing and state-of-the-art scaffolding protocols to generate, to our knowledge, the first reference-quality genomes of six bat species (Rhinolophus ferrumequinum, Rousettus aegyptiacus, Phyllostomus discolor, Myotis myotis, Pipistrellus kuhlii and Molossus molossus). We integrated gene projections from our 'Tool to infer Orthologs from Genome Alignments' (TOGA) software with de novo and homology gene predictions as well as short- and long-read transcriptomics to generate highly complete gene annotations. To resolve the phylogenetic position of bats within Laurasiatheria, we applied several phylogenetic methods to comprehensive sets of orthologous protein-coding and noncoding regions of the genome, and identified a basal origin for bats within Scrotifera. Our genome-wide screens revealed positive selection on hearing-related genes in the ancestral branch of bats, which is indicative of laryngeal echolocation being an ancestral trait in this clade. We found selection and loss of immunity-related genes (including pro-inflammatory NF-κB regulators) and expansions of anti-viral APOBEC3 genes, which highlights molecular mechanisms that may contribute to the exceptional immunity of bats. Genomic integrations of diverse viruses provide a genomic record of historical tolerance to viral infection in bats. Finally, we found and experimentally validated bat-specific variation in microRNAs, which may regulate bat-specific gene-expression programs. Our reference-quality bat genomes provide the resources required to uncover and validate the genomic basis of adaptations of bats, and stimulate new avenues of research that are directly relevant to human health and disease.
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http://dx.doi.org/10.1038/s41586-020-2486-3DOI Listing
July 2020

Genetic variation between long-lived versus short-lived bats illuminates the molecular signatures of longevity.

Aging (Albany NY) 2020 09;12(16):15962-15977

School of Biology and Environmental Science, University College Dublin, Belfield, Dublin, Ireland.

Bats are the longest-lived mammals given their body size with majority of species exhibiting exceptional longevity. However, there are some short-lived species that do not exhibit extended lifespans. Here we conducted a comparative genomic and transcriptomic study on long-lived (maximum lifespan = 37.1 years) and short-lived (maximum lifespan = 5.6 years) to ascertain the genetic difference underlying their divergent longevities. Genome-wide selection tests on 12,467 single-copy genes between and revealed only three genes (, and ) that exhibited significant positive selection. Although 97.96% of 12,467 genes underwent purifying selection, we observed a significant heterogeneity in their expression patterns. Using a linear mixed model, we obtained expression of 2,086 genes that may truly represent the genetic difference between and . Expression analysis indicated that long-lived exhibited a transcriptomic profile of enhanced DNA repair and autophagy pathways, compared to . Further investigation of the longevity-associated genes suggested that long-lived have naturally evolved a diminished anti-longevity transcriptomic profile. Together with observations from other long-lived species, our results suggest that heightened DNA repair and autophagy activity may represent a universal mechanism to achieve longevity in long-lived mammals.
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http://dx.doi.org/10.18632/aging.103725DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7485743PMC
September 2020

Broad Host Range of SARS-CoV-2 Predicted by Comparative and Structural Analysis of ACE2 in Vertebrates.

bioRxiv 2020 Apr 18. Epub 2020 Apr 18.

The Genome Center, University of California Davis, Davis, CA 95616, USA.

The novel coronavirus SARS-CoV-2 is the cause of Coronavirus Disease-2019 (COVID-19). The main receptor of SARS-CoV-2, angiotensin I converting enzyme 2 (ACE2), is now undergoing extensive scrutiny to understand the routes of transmission and sensitivity in different species. Here, we utilized a unique dataset of 410 vertebrates, including 252 mammals, to study cross-species conservation of ACE2 and its likelihood to function as a SARS-CoV-2 receptor. We designed a five-category ranking score based on the conservation properties of 25 amino acids important for the binding between receptor and virus, classifying all species from to . Only mammals fell into the to categories, and only catarrhine primates in the category, suggesting that they are at high risk for SARS-CoV-2 infection. We employed a protein structural analysis to qualitatively assess whether amino acid changes at variable residues would be likely to disrupt ACE2/SARS-CoV-2 binding, and found the number of predicted unfavorable changes significantly correlated with the binding score. Extending this analysis to human population data, we found only rare (<0.1%) variants in 10/25 binding sites. In addition, we observed evidence of positive selection in ACE2 in multiple species, including bats. Utilized appropriately, our results may lead to the identification of intermediate host species for SARS-CoV-2, justify the selection of animal models of COVID-19, and assist the conservation of animals both in native habitats and in human care.
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http://dx.doi.org/10.1101/2020.04.16.045302DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7263403PMC
April 2020

The Potential Role of Endogenous Viral Elements in the Evolution of Bats as Reservoirs for Zoonotic Viruses.

Annu Rev Virol 2020 09 20;7(1):103-119. Epub 2020 May 20.

Department of Zoology, University of Oxford, OX1 3PS Oxford, United Kingdom; email:

Despite a small genome size, bats have comparable diversity of retroviral and non-retroviral endogenous sequences to other mammals. These include Class I and Class II retroviral sequences, foamy viruses, and deltaretroviruses, as well as filovirus, bornavirus, and parvovirus endogenous viral elements. Some of these endogenous viruses are sufficiently preserved in bat genomes to be expressed, with potential effects for host biology. It is clear that the bat immune system differs when compared with other mammals, yet the role that virus-derived endogenous elements may have played in the evolution of bat immunity is poorly understood. In this review, we discuss some of the bat-specific immune mechanisms that may have resulted in a virus-tolerant phenotype and link these to the long-standing virus-host coevolution that may have allowed a large diversity of endogenous retroviruses and other endogenous viral elements to colonize bat genomes. We also consider the possible effects of endogenization in the evolution of the bat immune system.
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http://dx.doi.org/10.1146/annurev-virology-092818-015613DOI Listing
September 2020

Drivers of longitudinal telomere dynamics in a long-lived bat species, Myotis myotis.

Mol Ecol 2020 08 19;29(16):2963-2977. Epub 2020 Mar 19.

School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin, Ireland.

Age-related telomere shortening is considered a hallmark of the ageing process. However, a recent cross-sectional ageing study of relative telomere length (rTL) in bats failed to detect a relationship between rTL and age in the long-lived genus Myotis (M. myotis and M. bechsteinii), suggesting some other factors are responsible for driving telomere dynamics in these species. Here, we test if longitudinal rTL data show signatures of age-associated telomere attrition in M. myotis and differentiate which intrinsic or extrinsic factors are likely to drive telomere length dynamics. Using quantitative polymerase chain reaction, rTL was measured in 504 samples from a marked population, from Brittany, France, captured between 2013 and 2016. These represent 174 individuals with an age range of 0 to 7+ years. We find no significant relationship between rTL and age (p = .762), but demonstrate that within-individual rTL is highly variable from year to year. To investigate the heritability of rTL, a population pedigree (n = 1744) was constructed from genotype data generated from a 16-microsatellite multiplex, designed from an initial, low-coverage, Illumina genome for M. myotis. Heritability was estimated in a Bayesian, mixed model framework, and showed that little of the observed variance in rTL is heritable (h  = 0.01-0.06). Rather, correlations of first differences, correlating yearly changes in telomere length and weather variables, demonstrate that, during the spring transition, average temperature, minimum temperature, rainfall and windspeed correlate with changes in longitudinal telomere dynamics. As such, rTL may represent a useful biomarker to quantify the physiological impact of various environmental stressors in bats.
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http://dx.doi.org/10.1111/mec.15395DOI Listing
August 2020

Tissue Collection of Bats for -Omics Analyses and Primary Cell Culture.

J Vis Exp 2019 10 23(152). Epub 2019 Oct 23.

Department of Ecology & Evolution, Stony Brook University; Consortium for Inter-Disciplinary Environmental Research, Stony Brook University;

As high-throughput sequencing technologies advance, standardized methods for high quality tissue acquisition and preservation allow for the extension of these methods to non-model organisms. A series of protocols to optimize tissue collection from bats has been developed for a series of high-throughput sequencing approaches. Outlined here are protocols for the capture of bats, desired demographics to be collected for each bat, and optimized methods to minimize stress on a bat during tissue collection. Specifically outlined are methods for collecting and treating tissue to obtain (i) DNA for high molecular weight genomic analyses, (ii) RNA for tissue-specific transcriptomes, and (iii) proteins for proteomic-level analyses. Lastly, also outlined is a method to avoid lethal sampling by creating viable primary cell cultures from wing clips. A central motivation of these methods is to maximize the amount of potential molecular and morphological data for each bat and suggest optimal ways to preserve tissues so they retain their value as new methods develop in the future. This standardization has become particularly important as initiatives to sequence chromosome-level, error-free genomes of species across the world have emerged, in which multiple scientific parties are spearheading the sequencing of different taxonomic groups. The protocols outlined herein define the ideal tissue collection and tissue preservation methods for Bat1K, the consortium that is sequencing the genomes of every species of bat.
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http://dx.doi.org/10.3791/59505DOI Listing
October 2019

Longitudinal comparative transcriptomics reveals unique mechanisms underlying extended healthspan in bats.

Nat Ecol Evol 2019 07 10;3(7):1110-1120. Epub 2019 Jun 10.

School of Biology and Environmental Science, Science Centre West, University College Dublin, Dublin, Ireland.

Bats are the longest-lived mammals, given their body size. However, the underlying molecular mechanisms of their extended healthspans are poorly understood. To address this question we carried out an eight-year longitudinal study of ageing in long-lived bats (Myotis myotis). We deep-sequenced ~1.7 trillion base pairs of RNA from 150 blood samples collected from known aged bats to ascertain the age-related transcriptomic shifts and potential microRNA-directed regulation that occurred. We also compared ageing transcriptomic profiles between bats and other mammals by analysis of 298 longitudinal RNA sequencing datasets. Bats did not show the same transcriptomic changes with age as commonly observed in humans and other mammals, but rather exhibited a unique, age-related gene expression pattern associated with DNA repair, autophagy, immunity and tumour suppression that may drive their extended healthspans. We show that bats have naturally evolved transcriptomic signatures that are known to extend lifespan in model organisms, and identify novel genes not yet implicated in healthy ageing. We further show that bats' longevity profiles are partially regulated by microRNA, thus providing novel regulatory targets and pathways for future ageing intervention studies. These results further disentangle the ageing process by highlighting which ageing pathways contribute most to healthy ageing in mammals.
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http://dx.doi.org/10.1038/s41559-019-0913-3DOI Listing
July 2019

Cryptic diversity within the Megophrys major species group (Amphibia: Megophryidae) of the Asian Horned Frogs: Phylogenetic perspectives and a taxonomic revision of South Asian taxa, with descriptions of four new species.

Zootaxa 2018 Nov 18;4523(1):1-96. Epub 2018 Nov 18.

School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland Systematics Lab, Department of Environmental Studies, University of Delhi, Delhi, India Department of Life Sciences, The Natural History Museum, London SW7 5BD, UK.

The Megophrys major species group (MMSG) is composed of typically medium to large sized frogs. Within the genus, it is the most geographically widespread clade ranging from the western Himalayas to southern Indochina. In this study, we examined in detail the extent of cryptic diversity within the MMSG-Indian populations based on molecular data (up to ten genes) using multigene concatenation and coalescent-based phylogenetic techniques, species delimitation analyses and extensive morphological data.Molecular evidence suggests a high level of hidden cryptic diversity within the MMSG, particularly within the M. major species complex (MMC), highlighting overlapping distributions, a case of potential mitochondrial transfer between two species, and tree topology discordance between phylogenetic methods and mitochondrial and nuclear data sets. Most analyses indicated distinct eastern and western clades in the MMC, and that the western clade may further divide into a northern and a southern subclade.A detailed taxonomic review of Indian members of the Megophrys major species group is provided. Previously undocumented complex nomenclatural issues involving known species are highlighted and resolved. Megophrys monticola is taxonomically redefined for the first time as a valid species since its synonymy with M. parva in 1893. The taxonomic status of two recently described species, Xenophrys katabhako and X. sanu are discussed in light of increased molecular and morphological sampling, and are synonymised with M. monticola. Megophrys monticola and M. robusta are redescribed based on their original type specimens and recently collected material. Megophrys major is neotypified and M. robusta lectotypified to remove prevailing nomenclatural instability. Four new large sized Indian MMC species are formally described from the Northeast Indian states of Arunachal Pradesh, Meghalaya and Nagaland, and Myanmar. All South Asian MMSG species are morphologically diagnosed from known congeners in the group. The geographic distributions of all taxa discussed are significantly redefined based on the revised taxonomy and extensive literature review. Morphological and molecular evidence suggests that Megophrys major sensu stricto might be endemic to Northeast India; M. glandulosa is formally removed from the Indian and Bhutan species checklists. Numerous misidentifications in literature are highlighted and corrected. In order to reduce future misidentifications of species reported from surrounding regions, high definition images of the holotypes of three Chinese species, M. glandulosa, M. medogensis and M. zhangi are provided for the first time, and a detailed description of Myanmar specimens of M. glandulosa is also given. This study provides the principle foundation for further research into the taxonomic status of the remaining, currently undescribed MMC taxa from Southeast Asia.
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http://dx.doi.org/10.11646/zootaxa.4523.1.1DOI Listing
November 2018

As Blind as a Bat? Opsin Phylogenetics Illuminates the Evolution of Color Vision in Bats.

Mol Biol Evol 2019 01;36(1):54-68

UCD School of Biology and Environmental Science, University College Dublin, Dublin 4, Ireland.

Through their unique use of sophisticated laryngeal echolocation bats are considered sensory specialists amongst mammals and represent an excellent model in which to explore sensory perception. Although several studies have shown that the evolution of vision is linked to ecological niche adaptation in other mammalian lineages, this has not yet been fully explored in bats. Recent molecular analysis of the opsin genes, which encode the photosensitive pigments underpinning color vision, have implicated high-duty cycle (HDC) echolocation and the adoption of cave roosting habits in the degeneration of color vision in bats. However, insufficient sampling of relevant taxa has hindered definitive testing of these hypotheses. To address this, novel sequence data was generated for the SWS1 and MWS/LWS opsin genes and combined with existing data to comprehensively sample species representing diverse echolocation types and niches (SWS1 n = 115; MWS/LWS n = 45). A combination of phylogenetic analysis, ancestral state reconstruction, and selective pressure analyses were used to reconstruct the evolution of these visual pigments in bats and revealed that although both genes are evolving under purifying selection in bats, MWS/LWS is highly conserved but SWS1 is highly variable. Spectral tuning analyses revealed that MWS/LWS opsin is tuned to a long wavelength, 555-560 nm in the bat ancestor and the majority of extant taxa. The presence of UV vision in bats is supported by our spectral tuning analysis, but phylogenetic analyses demonstrated that the SWS1 opsin gene has undergone pseudogenization in several lineages. We do not find support for a link between the evolution of HDC echolocation and the pseudogenization of the SWS1 gene in bats, instead we show the SWS1 opsin is functional in the HDC echolocator, Pteronotus parnellii. Pseudogenization of the SWS1 is correlated with cave roosting habits in the majority of pteropodid species. Together these results demonstrate that the loss of UV vision in bats is more widespread than was previously considered and further elucidate the role of ecological niche specialization in the evolution of vision in bats.
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http://dx.doi.org/10.1093/molbev/msy192DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6340466PMC
January 2019

Population level mitogenomics of long-lived bats reveals dynamic heteroplasmy and challenges the Free Radical Theory of Ageing.

Sci Rep 2018 09 11;8(1):13634. Epub 2018 Sep 11.

School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland.

Bats are the only mammals capable of true, powered flight, which drives an extremely high metabolic rate. The "Free Radical Theory of Ageing" (FTRA) posits that a high metabolic rate causes mitochondrial heteroplasmy and the progressive ageing phenotype. Contrary to this, bats are the longest-lived order of mammals given their small size and high metabolic rate. To investigate if bats exhibit increased mitochondrial heteroplasmy with age, we performed targeted, deep sequencing of mitogenomes and measured point heteroplasmy in wild, long lived Myotis myotis. Blood was sampled from 195 individuals, aged between <1 and at 6+ years old, and whole mitochondria deep-sequenced, with a subset sampled over multiple years. The majority of heteroplasmies were at a low frequency and were transitions. Oxidative mutations were present in only a small number of individuals, suggesting local oxidative stress events. Cohort data showed no significant increase in heteroplasmy with age, while longitudinal data from recaptured individuals showed heteroplasmy is dynamic, and does not increase uniformly over time. We show that bats do not suffer from the predicted, inevitable increase in heteroplasmy as posited by the FRTA, instead heteroplasmy was found to be dynamic, questioning its presumed role as a primary driver of ageing.
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http://dx.doi.org/10.1038/s41598-018-31093-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6134106PMC
September 2018

AGILE: an assembled genome mining pipeline.

Bioinformatics 2019 04;35(7):1252-1254

School of Biology and Environmental Science, University College Dublin, Dublin 4, Ireland.

Summary: A number of limiting factors mean that traditional genome annotation tools either fail or perform sub-optimally when trying to detect coding sequences in poor quality genome assemblies/genome reports. This means that potentially useful data is accessible only to those with specific skills and expertise in assembly and annotation. We present an Assembled-Genome mIning pipeLinE (AGILE) written in Perl that combines bioinformatics tools with a number of steps to overcome the limitations imposed by such assemblies when applied to highly fragmented genomes. Our methodology uses user-specified query genes from a closely related species to mine and annotate coding sequences that would traditionally be missed by standard annotation packages. Despite a focus on mammalian genomes, the generalized implementation means that it may be applied to any genome assembly, providing a means for non-specialists to gather gene sequences for downstream analyses.

Availability And Implementation: Source code and associated files are available at: https://github.com/batlabucd/GenomeMining and https://bitbucket.org/BatlabUCD/genomemining/src. Singularity and Virtual Box images available at https://figshare.com/s/a0004bf93dc43484b0c0.

Supplementary Information: Supplementary data are available at Bioinformatics online.
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http://dx.doi.org/10.1093/bioinformatics/bty781DOI Listing
April 2019

The Birth and Death of Olfactory Receptor Gene Families in Mammalian Niche Adaptation.

Mol Biol Evol 2018 06;35(6):1390-1406

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

The olfactory receptor (OR) gene families, which govern mammalian olfaction, have undergone extensive expansion and contraction through duplication and pseudogenization. Previous studies have shown that broadly defined environmental adaptations (e.g., terrestrial vs. aquatic) are correlated with the number of functional and non-functional OR genes retained. However, to date, no study has examined species-specific gene duplications in multiple phylogenetically divergent mammals to elucidate OR evolution and adaptation. Here, we identify the OR gene families driving adaptation to different ecological niches by mapping the fate of species-specific gene duplications in the OR repertoire of 94 diverse mammalian taxa, using molecular phylogenomic methods. We analyze >70,000 OR gene sequences mined from whole genomes, generated from novel amplicon sequencing data, and collated with data from previous studies, comprising one of the largest OR studies to date. For the first time, we demonstrate statistically significant patterns of OR species-specific gene duplications associated with the presence of a functioning vomeronasal organ. With respect to dietary niche, we uncover a novel link between a large number of duplications in OR family 5/8/9 and herbivory. Our results also highlight differences between social and solitary niches, indicating that a greater OR repertoire expansion may be associated with a solitary lifestyle. This study demonstrates the utility of species-specific duplications in elucidating gene family evolution, revealing how the OR repertoire has undergone expansion and contraction with respect to a number of ecological adaptations in mammals.
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http://dx.doi.org/10.1093/molbev/msy028DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5967467PMC
June 2018

Growing old, yet staying young: The role of telomeres in bats' exceptional longevity.

Sci Adv 2018 02 7;4(2):eaao0926. Epub 2018 Feb 7.

School of Biology and Environmental Science, Science Centre West, University College Dublin, Belfield, Dublin 4, Ireland.

Understanding aging is a grand challenge in biology. Exceptionally long-lived animals have mechanisms that underpin extreme longevity. Telomeres are protective nucleotide repeats on chromosome tips that shorten with cell division, potentially limiting life span. Bats are the longest-lived mammals for their size, but it is unknown whether their telomeres shorten. Using >60 years of cumulative mark-recapture field data, we show that telomeres shorten with age in and , but not in the bat genus with greatest longevity, . As in humans, telomerase is not expressed in blood or fibroblasts. Selection tests on telomere maintenance genes show that and , which repair and prevent DNA damage, potentially mediate telomere dynamics in bats. Twenty-one telomere maintenance genes are differentially expressed in , of which 14 are enriched for DNA repair, and 5 for alternative telomere-lengthening mechanisms. We demonstrate how telomeres, telomerase, and DNA repair genes have contributed to the evolution of exceptional longevity in bats, advancing our understanding of healthy aging.
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http://dx.doi.org/10.1126/sciadv.aao0926DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5810611PMC
February 2018

Is there a link between aging and microbiome diversity in exceptional mammalian longevity?

PeerJ 2018 8;6:e4174. Epub 2018 Jan 8.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

A changing microbiome has been linked to biological aging in mice and humans, suggesting a possible role of gut flora in pathogenic aging phenotypes. Many bat species have exceptional longevity given their body size and some can live up to ten times longer than expected with little signs of aging. This study explores the anal microbiome of the exceptionally long-lived bat, investigating bacterial composition in both adult and juvenile bats to determine if the microbiome changes with age in a wild, long-lived non-model organism, using non-lethal sampling. The anal microbiome was sequenced using metabarcoding in more than 50 individuals, finding no significant difference between the composition of juvenile and adult bats, suggesting that age-related microbial shifts previously observed in other mammals may not be present in . Functional gene categories, inferred from metabarcoding data, expressed in the microbiome were categorized identifying pathways involved in metabolism, DNA repair and oxidative phosphorylation. We highlight an abundance of 'Proteobacteria' relative to other mammals, with similar patterns compared to other bat microbiomes. Our results suggest that may have a relatively stable, unchanging microbiome playing a role in their extended 'health spans' with the advancement of age, and suggest a potential link between microbiome and sustained, powered flight.
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http://dx.doi.org/10.7717/peerj.4174DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5764031PMC
January 2018

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species.

Annu Rev Anim Biosci 2018 02 20;6:23-46. Epub 2017 Nov 20.

*Full list of Bat1K Consortium members in Supplemental Appendix.

Bats are unique among mammals, possessing some of the rarest mammalian adaptations, including true self-powered flight, laryngeal echolocation, exceptional longevity, unique immunity, contracted genomes, and vocal learning. They provide key ecosystem services, pollinating tropical plants, dispersing seeds, and controlling insect pest populations, thus driving healthy ecosystems. They account for more than 20% of all living mammalian diversity, and their crown-group evolutionary history dates back to the Eocene. Despite their great numbers and diversity, many species are threatened and endangered. Here we announce Bat1K, an initiative to sequence the genomes of all living bat species (n∼1,300) to chromosome-level assembly. The Bat1K genome consortium unites bat biologists (>148 members as of writing), computational scientists, conservation organizations, genome technologists, and any interested individuals committed to a better understanding of the genetic and evolutionary mechanisms that underlie the unique adaptations of bats. Our aim is to catalog the unique genetic diversity present in all living bats to better understand the molecular basis of their unique adaptations; uncover their evolutionary history; link genotype with phenotype; and ultimately better understand, promote, and conserve bats. Here we review the unique adaptations of bats and highlight how chromosome-level genome assemblies can uncover the molecular basis of these traits. We present a novel sequencing and assembly strategy and review the striking societal and scientific benefits that will result from the Bat1K initiative.
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http://dx.doi.org/10.1146/annurev-animal-022516-022811DOI Listing
February 2018

ExUTR: a novel pipeline for large-scale prediction of 3'-UTR sequences from NGS data.

BMC Genomics 2017 Nov 6;18(1):847. Epub 2017 Nov 6.

UCD School of Biology and Environmental Science, University College Dublin, Belfield, Dublin 4, Ireland.

Background: The three prime untranslated region (3'-UTR) is known to play a pivotal role in modulating gene expression by determining the fate of mRNA. Many crucial developmental events, such as mammalian spermatogenesis, tissue patterning, sex determination and neurogenesis, rely heavily on post-transcriptional regulation by the 3'-UTR. However, 3'-UTR biology seems to be a relatively untapped field, with only limited tools and 3'-UTR resources available. To elucidate the regulatory mechanisms of the 3'-UTR on gene expression, firstly the 3'-UTR sequences must be identified. Current 3'-UTR mining tools, such as GETUTR, 3USS and UTRscan, all depend on a well-annotated reference genome or curated 3'-UTR sequences, which hinders their application on a myriad of non-model organisms where the genomes are not available. To address these issues, the establishment of an NGS-based, automated pipeline is urgently needed for genome-wide 3'-UTR prediction in the absence of reference genomes.

Results: Here, we propose ExUTR, a novel NGS-based pipeline to predict and retrieve 3'-UTR sequences from RNA-Seq experiments, particularly designed for non-model species lacking well-annotated genomes. This pipeline integrates cutting-edge bioinformatics tools, databases (Uniprot and UTRdb) and novel in-house Perl scripts, implementing a fully automated workflow. By taking transcriptome assemblies as inputs, this pipeline identifies 3'-UTR signals based primarily on the intrinsic features of transcripts, and outputs predicted 3'-UTR candidates together with associated annotations. In addition, ExUTR only requires minimal computational resources, which facilitates its implementation on a standard desktop computer with reasonable runtime, making it affordable to use for most laboratories. We also demonstrate the functionality and extensibility of this pipeline using publically available RNA-Seq data from both model and non-model species, and further validate the accuracy of predicted 3'-UTR using both well-characterized 3'-UTR resources and 3P-Seq data.

Conclusions: ExUTR is a practical and powerful workflow that enables rapid genome-wide 3'-UTR discovery from NGS data. The candidates predicted through this pipeline will further advance the study of miRNA target prediction, cis elements in 3'-UTR and the evolution and biology of 3'-UTRs. Being independent of a well-annotated reference genome will dramatically expand its application to much broader research area, encompassing all species for which RNA-Seq is available.
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http://dx.doi.org/10.1186/s12864-017-4241-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5674806PMC
November 2017

Identification of the same polyomavirus species in different African horseshoe bat species is indicative of short-range host-switching events.

J Gen Virol 2017 11 6;98(11):2771-2785. Epub 2017 Oct 6.

Global Virus Network, Baltimore, MD 21201, USA.

Polyomaviruses (PyVs) are considered to be highly host-specific in different mammalian species, with no well-supported evidence for host-switching events. We examined the species diversity and host specificity of PyVs in horseshoe bats (Rhinolophus spp.), a broadly distributed and highly speciose mammalian genus. We annotated six PyV genomes, comprising four new PyV species, based on pairwise identity within the large T antigen (LTAg) coding region. Phylogenetic comparisons revealed two instances of highly related PyV species, one in each of the Alphapolyomavirus and Betapolyomavirus genera, present in different horseshoe bat host species (Rhinolophus blasii and R. simulator), suggestive of short-range host-switching events. The two pairs of Rhinolophus PyVs in different horseshoe bat host species were 99.9 and 88.8 % identical with each other over their respective LTAg coding sequences and thus constitute the same virus species. To corroborate the species identification of the bat hosts, we analysed mitochondrial cytb and a large nuclear intron dataset derived from six independent and neutrally evolving loci for bat taxa of interest. Bayesian estimates of the ages of the most recent common ancestors suggested that the near-identical and more distantly related PyV species diverged approximately 9.1E4 (5E3-2.8E5) and 9.9E6 (4E6-18E6) years before the present, respectively, in contrast to the divergence times of the bat host species: 12.4E6 (10.4E6-15.4E6). Our findings provide evidence that short-range host-switching of PyVs is possible in horseshoe bats, suggesting that PyV transmission between closely related mammalian species can occur.
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http://dx.doi.org/10.1099/jgv.0.000935DOI Listing
November 2017

Prenatal development supports a single origin of laryngeal echolocation in bats.

Nat Ecol Evol 2017 Jan 9;1(2):21. Epub 2017 Jan 9.

Key Laboratory of Zoonosis of Liaoning Province, College of Animal Science and Veterinary Medicine, Shenyang Agricultural University, Shenyang 110866, China.

Bat laryngeal echolocation is considered as one of the most complex and diverse modes of auditory sensory perception in animals and its evolutionary history has been the cause of many scientific controversies in the past two decades. To date, the majority of scientific evidence supports that bats (Chiroptera) are divided into two subordinal groups: Yinpterochiroptera, containing the laryngeal echolocating superfamily Rhinolophidae as sister taxa to the non-laryngeal echolocating family Pteropodidae; and Yangochiroptera, containing all other laryngeal echolocating lineages. This topology has led to an unanswered question in mammalian biology: was laryngeal echolocation lost in the ancestral pteropodids or gained convergently in the echolocating bat lineages? To date, there is insufficient and conflicting evidence from fossil, genomic, morphological and phylogenomic data to resolve this question. We detail an ontogenetic study of fetal cochlear development from seven species of bats and five outgroup mammals and show that in early fetal development, all bats including the non-laryngeal echolocating pteropodids have a similarly large cochlea typically associated with laryngeal echolocation abilities. The subsequent cochlear growth rate in the pteropodids is the slowest of all mammals and leads to the pteropodids and the non-echolocating lineages eventually sharing a similar cochlear morphospace as adults. The results suggest that pteropodids maintain a vestigial developmental stage indicative of past echolocation capabilities and thus support a single origin of laryngeal echolocation in bats.
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http://dx.doi.org/10.1038/s41559-016-0021DOI Listing
January 2017

Genome-wide signatures of complex introgression and adaptive evolution in the big cats.

Sci Adv 2017 07 19;3(7):e1700299. Epub 2017 Jul 19.

Laboratório de Biologia Genômica e Molecular, Faculdade de Biociências, Pontifical Catholic University of Rio Grande do Sul (PUCRS), Porto Alegre, Rio Grande do Sul, Brazil.

The great cats of the genus comprise a recent radiation whose evolutionary history is poorly understood. Their rapid diversification poses challenges to resolving their phylogeny while offering opportunities to investigate the historical dynamics of adaptive divergence. We report the sequence, de novo assembly, and annotation of the jaguar () genome, a novel genome sequence for the leopard (), and comparative analyses encompassing all living species. Demographic reconstructions indicated that all of these species have experienced variable episodes of population decline during the Pleistocene, ultimately leading to small effective sizes in present-day genomes. We observed pervasive genealogical discordance across genomes, caused by both incomplete lineage sorting and complex patterns of historical interspecific hybridization. We identified multiple signatures of species-specific positive selection, affecting genes involved in craniofacial and limb development, protein metabolism, hypoxia, reproduction, pigmentation, and sensory perception. There was remarkable concordance in pathways enriched in genomic segments implicated in interspecies introgression and in positive selection, suggesting that these processes were connected. We tested this hypothesis by developing exome capture probes targeting ~19,000 genes and applying them to 30 wild-caught jaguars. We found at least two genes ( and , both related to optic nerve development) bearing significant signatures of interspecies introgression and within-species positive selection. These findings indicate that post-speciation admixture has contributed genetic material that facilitated the adaptive evolution of big cat lineages.
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http://dx.doi.org/10.1126/sciadv.1700299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5517113PMC
July 2017

The complete mitochondrial genome of the Bechstein's bat, (Chiroptera, Vespertilionidae).

Mitochondrial DNA B Resour 2017 Feb 16;2(1):92-94. Epub 2017 Feb 16.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

In this study, we present the complete mitochondrial genome of the Bechstein's bat, . The mitogenome is 17,151 bp in length and is AT-rich with base composition A (27.8%), C (22%), G (16.1%), and T (34.1%). The mitogenome shows conserved gene content and order similar with other mammalian mitogenomes, being composed of 13 protein-coding genes, 2 ribosomal RNA genes, 22 transfer RNA genes, and one control region. The majority of genes are encoded on the H-Strand except for and 8 tRNAs as found in other bat species. The field identification of was confirmed by phylogenetic analyses using datasets comprising whole mitogenomes and . This mitogenome is a resource for future studies of bats and other mammals.
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http://dx.doi.org/10.1080/23802359.2017.1280701DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7800535PMC
February 2017

Evolutionary History of the Asian Horned Frogs (Megophryinae): Integrative Approaches to Timetree Dating in the Absence of a Fossil Record.

Mol Biol Evol 2017 03;34(3):744-771

School of Biology and Environmental Science, University College Dublin, Belfield, Dublin, Ireland.

Molecular dating studies typically need fossils to calibrate the analyses. Unfortunately, the fossil record is extremely poor or presently nonexistent for many species groups, rendering such dating analysis difficult. One such group is the Asian horned frogs (Megophryinae). Sampling all generic nomina, we combined a novel ∼5 kb dataset composed of four nuclear and three mitochondrial gene fragments to produce a robust phylogeny, with an extensive external morphological study to produce a working taxonomy for the group. Expanding the molecular dataset to include out-groups of fossil-represented ancestral anuran families, we compared the priorless RelTime dating method with the widely used prior-based Bayesian timetree method, MCMCtree, utilizing a novel combination of fossil priors for anuran phylogenetic dating. The phylogeny was then subjected to ancestral phylogeographic analyses, and dating estimates were compared with likely biogeographic vicariant events. Phylogenetic analyses demonstrated that previously proposed systematic hypotheses were incorrect due to the paraphyly of genera. Molecular phylogenetic, morphological, and timetree results support the recognition of Megophryinae as a single genus, Megophrys, with a subgenus level classification. Timetree results using RelTime better corresponded with the known fossil record for the out-group anuran tree. For the priorless in-group, it also outperformed MCMCtree when node date estimates were compared with likely influential historical biogeographic events, providing novel insights into the evolutionary history of this pan-Asian anuran group. Given a relatively small molecular dataset, and limited prior knowledge, this study demonstrates that the computationally rapid RelTime dating tool may outperform more popular and complex prior reliant timetree methodologies.
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http://dx.doi.org/10.1093/molbev/msw267DOI Listing
March 2017

Blood miRNomes and transcriptomes reveal novel longevity mechanisms in the long-lived bat, Myotis myotis.

BMC Genomics 2016 11 10;17(1):906. Epub 2016 Nov 10.

UCD School of Biology and Environmental Science, University College Dublin, Belfield, Dublin, 4, Ireland.

Background: Chiroptera, the bats, are the only order of mammals capable of true self-powered flight. Bats exhibit a number of other exceptional traits such as echolocation, viral tolerance and, perhaps most puzzlingly, extreme longevity given their body size. Little is known about the molecular mechanisms driving their extended longevity particularly at the levels of gene expression and post-transcriptional regulation. To elucidate the molecular mechanisms that may underlie their unusual longevity, we have deep sequenced 246.5 million small RNA reads from whole blood of the long-lived greater mouse-eared bats, Myotis myotis, and conducted a series of genome-wide comparative analyses between bat and non-bat mammals (human, pig and cow) in both blood miRNomes and transcriptomes, for the first time.

Results: We identified 539 miRNA gene candidates from bats, of which 468 unique mature miRNA were obtained. More than half of these miRNA (65.1 %) were regarded as bat-specific, regulating genes involved in the immune, ageing and tumorigenesis pathways. We have also developed a stringent pipeline for genome-wide miRNome comparisons across species, and identified 37 orthologous miRNA groups shared with bat, human, pig and cow, 6 of which were differentially expressed. For bats, 3 out of 4 up-regulated miRNA (miR-101-3p, miR-16-5p, miR-143-3p) likely function as tumor suppressors against various kinds of cancers, while one down-regulated miRNA (miR-221-5p) acts as a tumorigenesis promoter in human breast and pancreatic cancers. Additionally, a genome-wide comparison of mRNA transcriptomes across species also revealed specific gene expression patterns in bats. 127 up-regulated genes were enriched mainly in mitotic cell cycle and DNA repair mechanisms, while 364 down-regulated genes were involved primarily in mitochondrial activity.

Conclusions: Our comprehensive and integrative analyses revealed bat-specific and differentially expressed miRNA and mRNA that function in key longevity pathways, producing a distinct bat gene expression pattern. For the first time, we show that bats may possess unique regulatory mechanisms for resisting tumorigenesis, repairing cellular damage and preventing oxidative stresses, all of which likely contribute to the extraordinary lifespan of Myotis myotis.
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http://dx.doi.org/10.1186/s12864-016-3227-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5103334PMC
November 2016

Patterns of orofacial clefting in the facial morphology of bats: a possible naturally occurring model of cleft palate.

J Anat 2016 11 27;229(5):657-672. Epub 2016 Jun 27.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

A normal feature of the facial anatomy of many species of bat is the presence of bony discontinuities or clefts, which bear a remarkable similarity to orofacial clefts that occur in humans as a congenital pathology. These clefts occur in two forms: a midline cleft between the two premaxillae (analogous to the rare midline craniofacial clefts in humans) and bilateral paramedian clefts between the premaxilla and the maxillae (analogous to the typical cleft lip and palate in humans). Here, we describe the distribution of orofacial clefting across major bat clades, exploring the relationship of the different patterns of clefting to feeding mode, development of the vomeronasal organ, development of the nasolacrimal duct and mode of emission of the echolocation call in different bat groups. We also present the results of detailed radiographic and soft tissue dissections of representative examples of the two types of cleft. The midline cleft has arisen independently multiple times in bat phylogeny, whereas the paramedian cleft has arisen once and is a synapomorphy uniting the Rhinolophidae and Hipposideridae. In all cases examined, the bony cleft is filled in by a robust fibrous membrane, continuous with the periosteum of the margins of the cleft. In the paramedian clefts, this membrane splits to enclose the premaxilla but forms a loose fold laterally between the premaxilla and maxilla, allowing the premaxilla and nose-leaf to pivot dorsoventrally in the sagittal plane under the action of facial muscles attached to the nasal cartilages. It is possible that this is a specific adaptation for echolocation and/or aerial insectivory. Given the shared embryological location of orofacial clefts in bats and humans, it is likely that aspects of the developmental control networks that produce cleft lip and palate in humans may also be implicated in the formation of these clefts as a normal feature in some bats. A better understanding of craniofacial development in bats with and without clefts may therefore suggest avenues for research into abnormal craniofacial development in humans.
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http://dx.doi.org/10.1111/joa.12510DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5055088PMC
November 2016

Wing Membrane Biopsies for Bat Cytogenetics: Finding of 2n = 54 in Irish Rhinolophushipposideros (Rhinolophidae, Chiroptera, Mammalia) Supports Two Geographically Separated Chromosomal Variants in Europe.

Cytogenet Genome Res 2016 23;148(4):279-83. Epub 2016 Jun 23.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

In Europe, 2 different diploid chromosome numbers, 2n = 54 and 2n = 56, have been described in the lesser horseshoe bat (Rhinolophushipposideros). The eastern form with 2n = 56 extends from the Czech Republic to Greece. To date, specimens with 54 chromosomes have been reported only from Spain and Germany. This study expands the distributional area of the western variant to Ireland. Strikingly, this distribution of European chromosomal variants is in contrast to the available molecular data that indicate little genetic differentiation of R. hipposideros populations spanning Northwestern to Central Europe. Further, we have developed an optimized protocol for establishing fibroblast cell cultures, suitable for karyotype analyses, from 3-mm wing membrane biopsies. This is a useful technique for cytogenetic studies of endangered bat species, as this non-lethal sampling method imposes only minimum stress to the animal without lasting adverse effects and is routinely used to sample tissue probes for molecular genetic studies in bats.
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http://dx.doi.org/10.1159/000447111DOI Listing
January 2017

Mammal madness: is the mammal tree of life not yet resolved?

Philos Trans R Soc Lond B Biol Sci 2016 07;371(1699)

School of Biology and Environmental Science, Science Centre East, University College Dublin, Dublin 4, Ireland

Most molecular phylogenetic studies place all placental mammals into four superordinal groups, Laurasiatheria (e.g. dogs, bats, whales), Euarchontoglires (e.g. humans, rodents, colugos), Xenarthra (e.g. armadillos, anteaters) and Afrotheria (e.g. elephants, sea cows, tenrecs), and estimate that these clades last shared a common ancestor 90-110 million years ago. This phylogeny has provided a framework for numerous functional and comparative studies. Despite the high level of congruence among most molecular studies, questions still remain regarding the position and divergence time of the root of placental mammals, and certain 'hard nodes' such as the Laurasiatheria polytomy and Paenungulata that seem impossible to resolve. Here, we explore recent consensus and conflict among mammalian phylogenetic studies and explore the reasons for the remaining conflicts. The question of whether the mammal tree of life is or can be ever resolved is also addressed.This article is part of the themed issue 'Dating species divergences using rocks and clocks'.
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http://dx.doi.org/10.1098/rstb.2015.0140DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4920340PMC
July 2016

The complete mitochondrial genome of Kuhl's pipistrelle, (Chiroptera: Vespertilionidae).

Mitochondrial DNA B Resour 2016 Jun 21;1(1):423-424. Epub 2016 Jun 21.

School of Biology and Environmental Science, University College Dublin, Dublin, Ireland.

The Kuhl's pipistrelle () is a small, vespertilionid bat species, with a large range extending from the Iberian Peninsula into the Near East and the Arabian Peninsula. In this study, we determine for the first time the complete mitogenome of this species. The mitogenome is 16,991 base pairs long with 37 genes and 1 control region, showing conserved gene content and order with other vertebrate mitogenomes. The length of the 22 tRNA genes ranges between 60 bp (tRNA-Ser) and 75 bp (tRNA-Leu). The D-loop region is 1553 bp long with low CG content (39.8%).
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http://dx.doi.org/10.1080/23802359.2016.1176886DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7799936PMC
June 2016