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Biology subjects

Teeling, E. C.

Publications and source records attributed to Teeling, E. C..

13 recordsLinked to original sources

Bat-mediated pest regulation in understudied pasture agroecosystems

Pastureland provides critical resources for livestock production. Despite the growing knowledge on pest regulating services provided by insectivorous bats, their role in pastureland systems remains understudied. We analysed the diets of four Irish bat species, Plecotus auritus, Pipistrellus pygmaeus, Myotis nattereri, and Rhinolophus hipposideros, to identify and categorise agricultural pest species based on metabarcoding studies in the pastureland rich agro-ecosystems of Ireland. Pest richness varied among bat species, with P. auritus consuming 22 known pest species, 13 in P. pygmaeus, 9 in R. hipposideros, and 7 in M. nattereri. Pest occurrence frequency varied in overall diets: R. hipposideros exhibited the highest (83%), followed by P. auritus (71%), M. nattereri (59%), and P. pygmaeus (32%). Importantly, 26 of the 35 pest species (74%) were consumed by only one bat species. Key pastureland pests, Tipula oleracea and T. paludosa, were detected across all bat species, with frequency of occurrence reaching up to 100% at several roosts. Livestock-associated disease vectors (Culicoides scoticus and C. pulicaris) were also consumed. Differences in diet among species reflect complementary foraging strategies, activity patterns, and habitat use, highlighting the collective role of bat communities in pest regulation. These findings provide additional evidence that insectivorous bats contribute to ecosystem services in pasturelands, potentially supporting reductions in pesticide use and enhancing sustainable pastureland management. By demonstrating the functional importance of bats beyond biodiversity conservation, this study underscores their value in nature-based solutions for sustainable agriculture and informs conservation and policy strategies in Ireland. Highlights- Clear habitat bias in studies of ecosystem services by insectivorous bats. - Bat species forage on diverse agricultural pests in pastureland-dominated areas. - Bat foraging behaviour influences consumption of specific pest species. - Bats consume major pasture pests, Tipula oleracea and T. paludosa. - Different bat species target different pests, enhancing overall control.

ecology↗

Early-life telomere length variation under changing developmental conditions in long-lived bats

Early-life conditions can shape molecular ageing processes, yet to what extent developmental variation in telomere length (TL) influences ageing trajectories remains unclear, particularly in long-lived mammals. We investigated how early-life environmental conditions and maternal age relate to juvenile TL and short-term survival in two long-lived bat species, Myotis myotis and Rhinolophus ferrumequinum. Using novel long-term datasets spanning ten years in M. myotis and five years in R. ferrumequinum, we measured relative telomere length (rTL) in juvenile wing tissue and applied sliding window analysis to identify sensitive climatic periods during development. In both species, early-life rTL varied significantly among years and was associated with short-term climatic conditions, with rainfall predicting rTL in both species and temperature acting in opposing directions: longer rTL with warmer conditions in M. myotis, and longer rTL at intermediate temperatures in R. ferrumequinum. Maternal age at conception showed little association with offspring TL in either species, although a weak positive sex-specific longitudinal effect was detected in R. ferrumequinum. Despite clear environmental influences on early-life rTL, we found no evidence that early-life rTL or early-life telomere change predicted short-term survival. Together, these results indicate that early-life telomere variation in bats reflects climatic conditions during development, providing novel insights into how early-life exposures could contribute to inter-individual differences in ageing trajectories in long-lived mammals.

molecular biology↗

Defying expectations: sex-biased telomere dynamics and extended lifespan in the tropical bat species, Molossus molossus.

Telomeres are key biomarkers of cellular ageing, yet their dynamics remain poorly studied in tropical and short-lived bat species. Here, we present the first investigation of telomere length across age in Molossus molossus, a tropical bat historically categorised as the shortest-lived bat on record. Through a multi-year mark-recapture study in Gamboa, Panama, we sampled 492 individuals (n = 317 females, 175 males) and documented a female M. molossus surviving to at least 13 years of age, more than doubling the previously reported maximum lifespan of 5.6 years. Across the population, relative telomere length (rTL) showed no overall significant decline with age. No evidence was found for sex-specific rates of telomere attrition. Rather these results suggest that males and females follow parallel age-related telomere trajectories, with any sex differences primarily reflecting differences in mean telomere length rather than ageing dynamics. Overall, the findings here challenge previous assumptions about the lifespan and ageing biology of M. molossus. They demonstrate that telomere maintenance is not limited to temperate bats, show that sex differences in telomere biology are subtle and species-specific, and reinforce the value of long-term field studies for understanding ageing processes in the wild.

molecular biology↗

Mating behaviour and connectivity drive sporadic European bat lyssavirus 2 infections in Myotis myotis

Gaining insight into the transmission and persistence of zoonoses in wild reservoirs is essential for preventing outbreaks, assessing demographic impacts, and informing conservation strategies. Achieving this requires reliable estimates of key epidemiological parameters, which are governed by aspects of host ecology and behaviour that are notoriously difficult to quantify in many wild species. Taking advantage of a long term study of the ecology of five Greater mouse-eared bats (Myotis myotis) maternity colonies in France ([~]2700 marked individuals), we sought to characterise lyssavirus infection dynamics in a wild bat reservoir. Although no lyssavirus was isolated from any of the 422 saliva samples tested, we report the first indirect evidence of European bat lyssavirus 2 circulation in this species. Interestingly, seropositivity appeared sporadic within colonies (0-100% annually) and synchronized across them, with highest seroprevalence in 2015-2017, but remaining low otherwise. Fitting Bayesian compartmental epidemiological models, we found that shifts in EBLV-2 prevalence were primarily driven by mating season introduction, age-dependant variation in transmission, and frequency-dependent transmission dynamics. Lyssavirus outbreaks involve few deaths overall but can still yield high annual mortality rates. These findings underscore the value of integrating ecological and individual-level data with mechanistic modelling to enhance our understanding and management of zoonotic pathogens in wildlife.

ecology↗

Metabarcoding reveals the effect of land cover and temporal variations on the diet of Brown long-eared and Soprano pipistrelle bats within a unique European habitat, the pasture dominated landscapes of Ireland.

Considered as tertiary keystone predators, insectivorous bats play essential roles in maintaining the functioning of ecosystems. Investigating how bat species diets vary across landscapes is crucial for understanding bat ecology and their role in ecosystem health. Here, we characterised the predator-prey interactions of two common bat species with different foraging strategies, the Brown long-eared bat (Plecotus auritus) and Soprano pipistrelle (Pipistrellus pygmaeus), across the unique pastureland dominated landscape of Ireland. Over three years (2021-2023), faecal samples (n=4,627 in total) were collected annually at three time points (gestation, lactation, post-lactation) from twelve maternity roosts and analysed using metabarcoding and next-generation sequencing. Both bat species showed broad diet diversity, with 392 and 350 arthropod species identified for Brown long-eared bat and Soprano pipistrelle, respectively, primarily Lepidoptera and Diptera. The Brown long-eared bat exhibited a generalist diet demonstrating dietary flexibility. Lepidoptera interactions were more frequent overall (62%) compared to Diptera (31%), but interactions with Diptera species increased markedly at one specific roost, highlighting its capacity to adjust its diet to local prey availability. In contrast, the Soprano pipistrelle exhibited a more specialised diet, with 83% consisting of Diptera species. Both spatial and temporal factors significantly influenced dietary richness and composition in both species. Surrounding land cover, in particular, played an important role in shaping diet composition. Our findings suggest that the Brown long-eared bat exhibits a broad foraging strategy, acting as a generalist with a preference for Lepidoptera, while the Soprano pipistrelle shows a consistent reliance on Diptera. This study underscores the reliance of two widespread bat species, which play an important role in ecosystem well-being, on diverse insect taxa, highlighting the urgent need to conserve these insect populations.

ecology↗

A comparative analysis of the antiviral response in two bat species reveals conserved and divergent innate immune pathways

Bats host a range of viruses that cause severe disease in humans without displaying clinical symptoms to these infections. The mechanisms of bat adaptation to these viruses are a continuous source of interest but remain largely unknown. To understand the landscape of bat antiviral response in a comprehensive and comparative manner, we studied this response in two bat species - the Egyptian fruit bat and the insectivore Kuhls pipistrelle, representing the two major bat subordinal clades. We profiled the transcriptional response to dsRNA - that triggers a rapid innate immune response - in skin fibroblasts from a large cohort of replicates from each bat species, using RNA-sequencing, and compared bat response with responses in primates and rodents. Both bat species upregulate a similar set of genes, many of which are known to be involved in the antiviral response across mammals. However, a subset of these genes is transcriptionally divergent in response between the two bat species. These transcriptionally divergent genes also evolve rapidly in coding sequence across the bat clade and have particular regulatory and functional characteristics, including specific promoter architectures and association with expression programs thought to underlie tolerance and resistance in response to viral infection. In addition, using single-cell transcriptomics, we show that transcriptionally divergent genes display high expression variability between individual cells. A focused analysis of dsRNA-sensing pathways further points to significant differences between bat and human in basal expression of genes important for triggering antiviral responses. Finally, a survey of genes recently lost or duplicated in bats points to a limited set of antiviral genes that have undergone rapid gene loss or gain in bats, with the latter group resulting in paralogs displaying divergence in both coding sequence and expression in bat tissues. Our study reveals a largely conserved regulatory program of genes upregulated in response to viral infection across bats and other mammals, and points to a set of genes that evolved rapidly in bats through multiple evolutionary mechanisms. This divergence can contribute to bat adaptation to viral infection and provides directions to understanding the mechanisms behind it.

evolutionary biology↗

Comparative genome microsynteny illuminates the fast evolution of nuclear mitochondrial segments (NUMTs) in mammals

The escape of DNA from mitochondria into the nuclear genome (nuclear mitochondrial DNA, NUMT) is an ongoing process. Although pervasively observed in eukaryotic genomes, their evolutionary trajectories in a mammal-wide context are poorly understood. The main challenge lies in the orthology assignment of NUMTs across species due to their fast evolution and chromosomal rearrangements over the past [~]200 million years. To address this issue, we systematically investigated the characteristics of NUMT insertions in 45 mammalian genomes, and established a novel, synteny-based method to accurately predict orthologous NUMTs and ascertain their evolution across mammals. With a series of comparative analyses across taxa, we revealed that NUMTs may originate from non-random regions in mtDNA, tend to locate in transposon-rich and intergenic regions, and unlikely code for functional proteins. Using our synteny-based approach, we leveraged 630 pairwise comparisons of genome-wide microsynteny and predicted the NUMT orthology relationships across 36 mammals. With the phylogenetic patterns of NUMT presence-and-absence across taxa, we constructed the ancestral state of NUMTs given the mammal tree using a coalescent method. We found support on the ancestral node of Fereuungulata within Laurasiatheria, whose subordinal relationships are still controversial. This strongly indicates that NUMT gain-and-loss over evolutionary time provides great insights into mammal evolution. However, we also demonstrated that one should be cautious when using ancestral NUMT trees to infer phylogenetic relationships. This study broadens our knowledge on NUMT insertion and evolution in mammalian genomes and highlights the merit of NUMTs as alternative genetic markers in phylogenetic inference.

evolutionary biology↗

Chiropterans are a hotspot for horizontal transfer of DNA transposons in Mammalia

Horizontal transfer of transposable elements is an important mechanism contributing to genetic diversity and innovation. Bats (order Chiroptera) have repeatedly been shown to experience horizontal transfer of transposable elements at what appears to be a high rate compared to other mammals. We investigated the occurrence of horizontally transferred DNA transposons involving bats. We found over 200 putative horizontally transferred elements within bats; sixteen transposons were shared across distantly related mammalian clades and two other elements were shared with a fish and two lizard species. Our results indicate that bats are a hotspot for horizontal transfer of DNA transposons. These events broadly coincide with the diversification of several bat clades, supporting the hypothesis that DNA transposon invasions have contributed to genetic diversification of bats.

molecular biology↗

Mark loss can strongly bias demographic rates in multi-state models: a case study with simulated and empirical datasets

O_LIThe development of methods for individual identification in wild species and the refinement of Capture-Mark-Recapture (CMR) models over the past few decades have greatly improved the assessment of population demographic rates to address ecological and conservation questions. In particular, multi-state models, which offer flexibility in analysing complex study systems, have gained popularity within the ecological community. In this study, we focus on the issue of mark loss and the associated recycling of remarked individuals, which requires further exploration given the increasing use of these models. C_LIO_LITo fill this knowledge gap, we employed a wide range of simulation scenarios that reflect commonly encountered real case studies, drawing inspiration from the survival rates of 700 vertebrate species. Using a multi-state, Arnason-Schwartz (AS) modelling framework, we estimated the effects of mark loss and recycled individuals on parameter estimates. We assessed parameter bias by simulating a metapopulation system with varying capture and survival rates. Additionally, we demonstrated how mark loss can be easily estimated and accounted for using a 10-year empirical CMR dataset of bats. The bats were individually identified using Passive Integrated Transponder (PIT) tag technology as potentially lost marks and multi-locus genotypes as permanent marks. C_LIO_LIOur simulation results revealed that the occurrence of bias and the affected parameters were highly dependent on the study system, making it difficult to establish general rules to predict bias a priori. The model structure and the interdependency among parameters pose challenges in predicting the impact of bias on estimates. C_LIO_LIOur findings underscore the importance of assessing the effect of mark loss when using AS models. Ignoring such violations of model assumptions can have significant implications for ecological inferences and conservation policies. In general, the use of permanent marks, such as genotypes, should always be preferred when modelling population dynamics. If that is not feasible, an alternative is to combine two independent types of temporary marks, such as PIT tags and bands. C_LIO_LIAnalysis of our empirical dataset on Myotis myotis bats revealed that tag loss is higher in juveniles than in adults during the first year after tagging. The use of surgical glue to close the injection hole reduces tag loss rate from 28% to 19% in juveniles, while it has no effect on the tag loss rate in adults ([~]10%). The main bias observed in our metapopulation system appears in the survival rate, with up to a 20% underestimation if tag loss is not accounted for. C_LI

ecology↗

Genome Methylation Predicts Age and Longevity of Bats

Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.

genomics↗

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

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 very high to very low. Only mammals fell into the medium to very high categories, and only catarrhine primates in 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 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.

genomics↗

Six new reference-quality bat genomes illuminate the molecular basis and evolution of bat adaptations

Bats account for ~20% of all extant mammal species and are considered exceptional given their extraordinary adaptations, including biosonar, true flight, extreme longevity, and unparalleled immune systems. To understand these adaptations, we generated reference-quality genomes of six species representing the key divergent lineages. We assembled these genomes with a novel pipeline incorporating state-of-the-art long-read and long-range sequencing and assembly techniques. The genomes were annotated using a maximal evidence approach, de novo predictions, protein/mRNA alignments, Iso-seq long read and RNA-seq short read transcripts, and gene projections from our new TOGA pipeline, retrieving virtually all (>99%) mammalian BUSCO genes. Phylogenetic analyses of 12,931 protein coding-genes and 10,857 conserved non-coding elements identified across 48 mammalian genomes helped to resolve bats closest extant relatives within Laurasiatheria, supporting a basal position for bats within Scrotifera. Genome-wide screens along the bat ancestral branch revealed (a) selection on hearing-involved genes (e.g LRP2, SERPINB6, TJP2), which suggest that laryngeal echolocation is a shared ancestral trait of bats; (b) selection (e.g INAVA, CXCL13, NPSR1) and loss of immunity related proteins (e.g. LRRC70, IL36G), including pro-inflammatory NF-kB signalling; and (c) expansion of the APOBEC family, associated with restricting viral infection, transposon activity and interferon signalling. We also identified unique integrated viruses, indicating that bats have a history of tolerating viral pathogens, lethal to other mammal species. Non-coding RNA analyses identified variant and novel microRNAs, revealing regulatory relationships that may contribute to phenotypic diversity in bats. Together, our reference-quality genomes, high-quality annotations, genome-wide screens and in-vitro tests revealed previously unknown genomic adaptations in bats that may explain their extraordinary traits.

genomics↗

Population level mitogenomics of the long-lived Greater Mouse-eared bat, Myotis myotis, reveals dynamic heteroplasmy and challenges the Free Radical Theory of Ageing

BackgroundBats 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 leads to mitochondrial heteroplasmy and the progressive ageing phenotype. Contrary to this, bats are the longest lived order of mammals despite their small size and high metabolic rate. To investigate if bats exhibit increased mitochondrial heteroplasmy with age as predicted by the FRTA, we performed targeted, deep sequencing of mitogenomes and measured point heteroplasmy in wild, long lived Myotis myotis as they age.\n\nResultsIn total, blood was sampled from 195 individuals, aged between <1 and at 6+ years old, and whole mitochondria were sequenced, with a subset sampled over multiple years. The majority of heteroplasmies, 77.6%, were at a frequency below 5%. Oxidative mutations were not the primary source of heteroplasmies and present in only a small number of individuals, likely representing local oxidative stress events. There was a significant positive correlation between age and heteroplasmy, with a rate of increase of 0.13 sites per year. Longitudinal data from recaptured individuals show heteroplasmy is dynamic, and does not increase uniformly over time.\n\nConclusionsWe show that bats do not suffer from the predicted, inevitable increase in heteroplasmy which underscores the FRTA. Most heteroplasmies were at low frequency and are primarily transitions. Heteroplasmy increased with age, however how this contributes to ageing is unclear, as heteroplasmy was dynamic, questioning its presumed role as a primary driver of ageing.

genomics↗