Biology subjects

Puechmaille, S. J.

Publications and source records attributed to Puechmaille, S. J..

11 recordsLinked to original sources

bioRxiv2026

A 10-year longitudinal study reveals bat-driven SARSr-CoV evolution

Bats are recognized reservoirs for several zoonoses and have an exceptional tolerance to viruses, likely linked with strong evolutionary selection in immune genes. Notably, in light of the emergence history of severe acute respiratory syndrome coronavirus (SARS-CoV), SARS-CoV-2 is hypothesized to have originated from Rhinolophus bats as well. In-depth studies are still needed, however, to unravel how SARS-related coronaviruses (SARSr-CoVs) persist and thrive in nature through evolution, virus-host interactions, and cross-species transmission. Here we present a pioneering 10-year longitudinal study of BBCoV-EPI1, a SARSr-CoV in Rhinolophus bats that revealed the complexity of virus-host interactions and the tempo at which new viral lineages emerge. Our results demonstrated the impacts of host life cycles (hibernation, female gathering, weaning juveniles, and mating periods) on strong seasonal oscillations in viral prevalence. These pronounced fluctuations drove viral diversification through bottlenecks, founder effects and Darwinian selection, counterbalanced by high mutation rates, fast gradualism, and recombination. We also found that host-cell enzymes are major contributors to BBCoV-EPI1 evolution in bats. The antiviral effect of APOBEC3 detected here in bats is weaker than it is in humans. Conversely, the ADAR enzyme had an unexpectedly strong and beneficial influence on viral evolution, even though the high mutation rate of RNA viruses is usually attributed to viral polymerases' low replication fidelity. We discovered that key BBCoV-EPI1 innovations in Rhinolophus bats were mostly located in proteins involved in cell-cycle hijack and in blocking bat cells' antiviral response, rather than in the Spike (S). We also showed that the BBCoV-EPI1 S protein efficiently uses angiotensin-converting enzyme 2 (ACE2) receptor to enter Rhinolophus bat cells, but not to enter human or sympatric species cells, due to amino-acid differences at the S-ACE2 interface. Last, this work identifies 101 critical amino-acid changes frequently associated with viral fitness shift, and paves the way for future experimental studies focusing on the capacity of SARSr-CoVs to adapt to hosts and cross the species barrier.

microbiology↗

bioRxiv2026

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↗

bioRxiv2025

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↗

bioRxiv2024

The geometry of gametic dispersal in a flying mammal, Rhinolophus hipposideros

Dispersal influences population and evolutionary dynamics, with effects that depend on the dispersal strategies through which gene flow occurs. In some species, mating partners move exclusively for mating, dispersing genes but not individuals. This is the case in many bat species, of which the lesser horseshoe bat (Rhinolophus hipposideros) shows a genetic structure at a fine spatial scale suggesting restricted dispersal. We investigated how natal and mating dispersal shape gene flow in this species in two metapopulations using paternity and population assignments. Half of the inferred paternities were intra-colonial and gave an estimate of the mean mating dispersal distance of around 11 km, explaining the observed genetic structure. Complete gametic dispersal distances were further estimated by combining natal with mating dispersal distances. The resulting gametic dispersal kernels showed a mean distance of around 20 km and a fat-tailed distribution typical of an excess of long-distance dispersal movements. It is the first time that natal and mating dispersal distances have been separately estimated and then combined in animals, documenting quantitatively how mating dispersal decorrelates gene and individual flows. It is important to consider this mechanism to explain dispersal evolution.

evolutionary biology↗

bioRxiv2023

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↗

bioRxiv2023

Climatic factors and host species composition at hibernation sites drive the incidence of bat fungal disease

Emerging infectious diseases pose a serious threat to wildlife, and their occurrence will likely be further exacerbated due to climate change. The aim of our study was to investigate whether the occurrence of White-nose disease (WND), a fungal disease of hibernating bats, can be predicted using local climatic conditions and host species abundance at hibernation sites. In addition, we used our model to predict areas potentially at risk if the pathogen is introduced and investigated how the potential distribution of WND may shift in the future due to climate change. We employed logistic regression as part of our ecological niche modelling approach, integrating climate and census data as explanatory variables, along with WND status (the response variable) obtained from 448 hibernacula. This approach allowed us to predict regions at elevated risk of WND by applying these climatic variables to current global climatic conditions and a climate change scenario. A model incorporating data on mean annual surface temperature, precipitation, and three host species reliably predicted WND occurrence in Europe. This model demonstrated robust transferability beyond Europe, as confirmed by both theoretical and empirical assessments (e.g., accurately predicting the observed mortality events in North America). We identified several high-risk areas in the southern hemisphere and demonstrate that climate change may cause a remarkable shift in the distribution range of WND. Our results highlight the importance of environmental factors in controlling the manifestation of disease in localities where both the pathogen and suitable hosts are present. We pinpoint several areas requiring increased surveillance and precautions to avoid the introduction of the pathogen, and show that climate change has massive potential to reshape and expand these areas, putting new populations at risk.

ecology↗

bioRxiv2022

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↗

bioRxiv2021

Population genetics as a tool to elucidate pathogen reservoirs: Lessons from Pseudogymnoascus destructans, the causative agent of white-nose disease in bats

Emerging infectious diseases pose a major threat to human, animal, and plant health. The risk of species-extinctions increases when pathogens can survive in the absence of the host, for example in environmental reservoirs. However, identifying such reservoirs and modes of infection is often highly challenging. In this study, we investigated the presence and nature of an environmental reservoir for the ascomycete fungus Pseudogymnoascus destructans, the causative agent of white-nose disease. We also characterised the modes and timing of transmission of the pathogen; key elements to better understand the disease dynamics. Using 18 microsatellite markers, we determined the genotypic and genic (based on allele frequencies) differentiation between 1,497 P. destructans isolates collected from nine closely situated hibernacula in North-Eastern Germany. One hibernaculum was the focus of intensive sampling in which both the bats and walls of the site were sampled at regular intervals over five consecutive winter seasons (1,062 isolates). We found significant genic differentiation between sites and few multi-locus genotypes shared across hibernacula (genotypic differentiation). This demonstrates that each hibernaculum has an essentially unique population of the fungus. This would be expected if bats purge viable P. destructans over the summer, preventing the mixing and exchange of the pathogen in maternity colonies, where bats from all of the studied hibernacula meet. Results from the intensively sampled site show higher measures of genotypic richness on walls compared to bats, the absence of genic differentiation between bats and walls, and stable relative abundance of multi-locus genotypes over multiple winter seasons. This clearly implicates hibernacula walls as the main environmental reservoir of the pathogen, from which bats become re-infected annually.

ecology↗

bioRxiv2019

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↗

bioRxiv2019

Population-level sensitivity to landscape variables reflects individual-based habitat selection in a woodland bat species

Understanding the relationship between habitat quality and population dynamics is fundamental for long-term management and range predictions in ecology. However, habitat quality is generally only investigated at the individual scale, as it is the case for the lesser horseshoe bat (Rhinolophus hipposideros), a species of conservation concern. Using a statistical modelling approach and census data of 94 lesser horseshoe bat colonies located in Brittany (France), we analysed the effect of landscape composition and configuration on the demographic components of surveyed maternity colonies (i.e. colony size, fecundity and growth rate), and compared our result to those provided by individual-based studies. Our results validated that the landscape in a 500-meter buffer around colonies (core foraging area) is crucial for population size and dynamics, and confirmed the positive influence of broadleaved woodland proportion on bat colony size. We revealed a positive effect of lakeshores and riverbanks on colony size and growth rate, underlying the importance of these habitats for the long-term conservation of this non-migratory forest species. Importantly, our results refine previous knowledge concerning the threat posed by the intensification of human activities (e.g. urbanization, agriculture, habitat fragmentation), and highlight the negative effect of large and regular patches of artificial and crop lands and of open land patches shape complexity on all demographic variables investigated. While our results support the dependence of population dynamics and associated conservation management to individual behaviour and sensitivity, environmental responses differed between the population metrics investigated, showing that efficient range prediction will require to fully grasp the complexity of the interaction between landscape and the different population dynamic parameters.

ecology↗

bioRxiv2017

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↗