Identifying the ecological and evolutionary factors that shape phage-bacterial interactions is key to understanding their dynamics in microbial communities. Yet, such interactions remain poorly characterised in plant agroecosystems. Here, we investigate the ecological determinants of the interaction between a highly diverse set of 23 phages isolated from diseased apricot trees and 44 bacterial strains from the Pseudomonas syringae species complex collected either from diseased apricot trees, healthy plants or non-agricultural environment. Based on their ecological origin, we expected phages to preferentially infect bacterial strains from the same ecological context, forming modular host-range patterns. Contrary to these expectations, we discovered a significantly nested structure, suggesting generalised infection dynamics rather than local adaptation, primarily driven by the broad ecological dynamics of this pathosystem. Analysis of the bacterial genomes showed that both the profiles of anti-phage defence systems and the distribution profiles of prophages are strongly shaped by bacterial phylogeny. Furthermore, while the number of defence systems showed limited correlation with the breadth of bacterial sensitivity to phages, prophage abundance exhibited a strong, non-linear link with phage virulence. Together, these findings provide an ecological and evolutionary perspective on phage-bacterium infection networks and new insights into a better understanding of the role of phages in agricultural ecosystems.
In a context of unprecedented insect decline, it is critical to have reliable monitoring tools to measure species diversity and their dynamic at large-scales. High-throughput DNA-based identification methods, and particularly metabarcoding, were proposed as an effective way to reach this aim. However, these identification methods are subject to multiple technical limitations, resulting in unavoidable false-positive and false-negative species detection. Moreover, metabarcoding does not allow a reliable estimation of species abundance in a given sample, which is key to document and detect population declines or range shifts at large scales. To overcome these obstacles, we propose here a human-assisted molecular identification (HAMI) approach, a framework based on a combination of metabarcoding and image-based parataxonomic validation of outputs and recording of abundance. We assessed the advantages of using HAMI over the exclusive use of a metabarcoding approach by examining 492 mixed beetle samples from a biodiversity monitoring initiative conducted throughout France. On average, 23% of the species are missed when relying exclusively on metabarcoding, this percent being consistently higher in species-rich samples. Importantly, on average, 20% of the species identified by molecular-only approaches correspond to false positives linked to cross-sample contaminations or mis-identified barcode sequences in databases. The combination of molecular methodologies and parataxonomic validation in HAMI significantly reduces the intrinsic biases of metabarcoding and recovers reliable abundance data. This approach also enables users to engage in a virtuous circle of database improvement through the identification of specimens associated with missing or incorrectly assigned barcodes. As such, HAMI fills an important gap in the toolbox available for fast and reliable biodiversity monitoring at large scales.
To better understand the emergence of cucumber mosaic virus (CMV) in the protected designation of origin of Espelette pepper (southwestern France), more than 7,300 samples were collected in and around 36 pepper fields in 2021 and 2022 and diagnosed using ELISA, RT-PCR, and partial Sanger sequencing of viral RNAs. This allowed the identification of five new host genera or species among the natural hosts of CMV: Arum italicum, Cerastium glomeratum, Hyacinthoides sp., Lysimachia arvensis, and Trifolium incarnatum. A CMV variant belonging to subgroup IB and presenting a low molecular diversity was highly prevalent in the pepper crops (78% of the pepper samples) as well as in naturally growing plants (8% of the non-pepper samples) within the fields. CMV isolates from group II were detected in a single pepper plant as well as in Hyacinthoides sp. (three samples), Capsella bursa-pastoris (two samples), and Stachys arvensis (one sample). To our knowledge, this is the second report of the occurrence of subgroup IB of CMV in France. Investigation of old pepper samples indicated that it has been present at least since 2009.
Implementing integrated pest management programs to limit agricultural pest damage requires an understanding of the interactions between the environmental variability and population demographic processes. However, identifying key environmental drivers of spatio-temporal pest population dynamics remains challenging as numerous candidate factors can operate at a range of scales, from the field (e.g. agricultural practices) to the regional scale (e.g. weather variability). In such a context, data- driven approaches applied to pre-existing data may allow identifying patterns, correlations, and trends that may not be apparent through more restricted hypothesis-driven studies. The resulting insights can lead to the generation of novel hypotheses and inform future experimental work focusing on a limited and relevant set of environmental predictors. In this study, we developed an ecoinformatics approach to unravel the multi-scale environmental conditions that lead to the early re-infestation of mango orchards by a major pest in Senegal, the oriental fruit fly Bactrocera dorsalis (BD). We gathered abundance data from a three-year monitoring conducted in 69 mango orchards as well as environmental data (i.e. orchard management, landscape structure and weather variability) across a range of spatial scales. We then developed a flexible analysis pipeline centred on a recent machine learning algorithm, which allows the combination of gradient boosting and grouped random effects models or Gaussian processes, to hierarchize the effects of multi-scale environmental variables on the onset of annual BD population growth in orchards. We found that physical factors (humidity, temperature), and to some extent landscape variables, were the main drivers of the spatio-temporal variability of the onset of population growth in orchards. These results suggest that favourable microclimate conditions could provide refuges for small BD populations that could survive, with little or no reproduction, during the mango off-season and, then, recolonize neighbouring orchards at the beginning of the next mango season. Confirmation of such a hypothesis could help to prioritize surveillance and preventive control actions in refuge areas.
Rivers, creeks, streams are integrators of biological, chemical and physical processes occurring in a catchment linking land cover from the headwaters to the outlet. The dynamics of human and animal pathogens in catchments have been widely studied in a large variety of contexts allowing the optimization of disease risk reduction. In parallel, there is an emerging awareness that crop pathogens might also be disseminated via surface waters especially when they are used for irrigation. However, there are no studies on the extent to which potential plant pathogens are present – nor about their dynamics - along the full course of a catchment. Here we have compared the seasonal dynamics of populations of the Pseudomonas syringae (Psy) and the Soft Rot Pectobacteriaceae (SRP) species complexes along a 270 km stretch of the Durance River from the upstream alpine reaches to the downstream agricultural production areas at the confluence with the Rhone River at Avignon. Among 168 samples collected at 21 sites in fall, winter, spring and summer of 2016 and 2017, Psy strains were detected at all sampling sites and in 156 of the samples at population densities up to 105 bacteria L-1. In contrast, SRP strains were detected in 98 of the samples, mostly from the southern part of the river, at population densities that did not exceed 3 ´ 104 bacteria L-1. Among the biological and chemical parameters that were characterized at each sampling site, temperature was the only factor that explained a significant amount of the variability in population size for both species complexes. Psy densities decreased with increasing temperature whereas SRP densities increased with increasing temperature. River-borne populations of SRP were composed mainly of Pectobacterium versatile and P. aquaticum that have little known epidemiological importance. Only a few strains of Pectobacterium and Dickeya species reputed for their epidemiological impact were observed. In contrast, Psy populations at all sites were dominated by a genetic lineage of phylogroup 2 known from other studies for its broad host range and its geographic and habitat ubiquity. Our observations suggest that surveillance of river water for SRP could be leveraged to signal diagnostic and management reactions to avoid disease outbreaks. In contrast, the constant presence of Psy throughout the catchment in absence of regular and widespread disease outbreaks due to this group of bacteria suggests that surveillance should focus on future changes in land use, river water conditions and agronomic practices that could destabilize the mechanisms currently holding Psy outbreaks in check.
Abstract Urbanization processes are taking place at a very high rate, especially in Africa. At the same time, a number of small mammal species, be they native or invasive, take advantage of human‐induced habitat modifications. They represent commensal communities of organisms that cause a number of inconveniences to humans, including potential reservoirs of zoonotic diseases. We studied via live trapping and habitat characterization such commensal small mammal communities in small villages to large cities of Senegal, to try to understand how the species share this particular space. Seven major species were recorded, with exotic invasive house mice (Mus musculus) and black rats (Rattus rattus) dominating in numbers. The shrew Crocidura olivieri appeared as the main and more widespread native species, while native rodent species (Mastomys natalensis, M. erythroleucus, Arvicanthis niloticus and Praomys daltoni) were less abundant and/or more localized. Habitat preferences, compared between species in terms of room types and characteristics, showed differences among house mice, black rats and M. natalensis especially. Niche (habitat component) breadth and overlap were measured. Among invasive species, the house mouse showed a larger niche breadth than the black rat, and overall, all species displayed high overlap values. Co‐occurrence patterns were studied at the global and local scales. The latter show cases of aggregation (between the black rat and native species, for instance) and of segregation (as between the house mouse and the black rat in Tambacounda, or between the black rat and M. natalensis in Kédougou). While updating information on commensal small mammal distribution in Senegal, a country submitted to a dynamic process of invasion by the black rat and the house mouse, we bring original information on how species occupy and share the commensal space, and make predictions on the evolution of these communities in a period of ever‐accelerating global changes.
ABSTRACTRivers, creeks, streams are integrators of biological, chemical and physical processes occurring in a catchment linking land cover from the headwaters to the outlet. The dynamics of human and animal pathogens in catchments have been widely studied in a large variety of contexts allowing the optimization of disease risk reduction. In parallel, there is an emerging awareness that crop pathogens might also be disseminated via surface waters especially when they are used for irrigation. However, there are no studies on the extent to which potential plant pathogens are present – nor about their dynamics - along the full course of a catchment. Here we have compared the seasonal dynamics of populations of thePseudomonas syringae(Psy) and the Soft RotPectobacteriaceae(SRP) species complexes along a 270 km stretch of the Durance River from the upstream alpine reaches to the downstream agricultural production areas at the confluence with the Rhone River at Avignon. Among 168 samples collected at 21 sites in fall, winter, spring and summer of 2016 and 2017, Psy strains were detected at all sampling sites and in 156 of the samples at population densities up to 105bacteria L−1. In contrast, SRP strains were detected in 98 of the samples, mostly from the southern part of the river, at population densities that did not exceed 3 × 104bacteria L−1. Among the biological and chemical parameters that were characterized at each sampling site, temperature was the only factor that explained a significant amount of the variability in population size for both species complexes. Psy densities decreased with increasing temperature whereas SRP densities increased with increasing temperature. River-borne populations of SRP were composed mainly ofPectobacterium versatileandP. aquaticumthat have little known epidemiological importance. Only a few strains ofPectobacteriumandDickeyaspecies reputed for their epidemiological impact were observed. In contrast, Psy populations at all sites were dominated by a genetic lineage of phylogroup 2 known from other studies for its broad host range and its geographic and habitat ubiquity. Our observations suggest that surveillance of river water for SRP could be leveraged to signal diagnostic and management reactions to avoid disease outbreaks. In contrast, the constant presence of Psy throughout the catchment in absence of regular and widespread disease outbreaks due to this group of bacteria suggests that surveillance should focus on future changes in land use, river water conditions and agronomic practices that could destabilize the mechanisms currently holding Psy outbreaks in check.
Population genetic approaches may be used to investigate dispersal patterns of species living in highly urbanized environment in order to improve management strategies for biodiversity conservation or pest control. However, in such environment, population genetic structure may reflect both current features of the cityscape and urbanization history. This can be especially relevant when focusing on exotic commensal rodents that have been introduced in numerous primary colonial European settlements. Accounting for spatial and temporal cityscape heterogeneity to determine how past and recent demographic events may interplay to shape current population genetic structure of synanthropic rodents may provide useful insights to manage their populations. In this study, we addressed these issues by focusing on the house mouse, Mus musculus domesticus, in Dakar, Senegal, where the species may have been introduced as soon as Europeans settled in the middle of the nineteenth century. We examined genetic variation at one mitochondrial locus and 15 nuclear microsatellite markers from individuals sampled in 14 sampling sites representing different stages of urbanization history and different socio-economic environments in Dakar. We used various approaches, including model-based genetic clustering and model-free smoothing of pairwise genetic estimates. We further linked observed spatial genetic patterns to historical and current features of Dakar cityscape using random forest and Bayesian conditional autoregressive models. Results are consistent with an introduction of the house mouse at colonial time and the current genetic structure exhibits a gradient-like pattern reflecting the historical process of spatially continuous expansion of the city from the first European settlement. The genetic patterns further suggest that population dynamics of the house mouse is also driven by the spatial heterogeneity of the current cityscape, including socio-economics features, that translate in habitat quality. Our results highlight the potential importance of accounting for past demographic events to understand spatial genetic patterns of nonnative invasive commensal rodents in highly urbanized environment.
Understanding the relationships between wildlife biodiversity and zoonotic infectious diseases in a changing climate is a challenging issue that scientists must address to support further policy actions. We aim at tackling this challenge by focusing on small mammal-borne diseases in temperate forests and large urban green spaces. Small mammals are important reservoirs of zoonotic agents, with a high transmission potential for humans and domestic animals. Forests and large urban green spaces are ecosystems where efforts are undertaken to preserve biodiversity. They are put forward for their contribution to human well-being in addition to other ecosystem services (e.g. provisioning and regulating services). Moreover, forests and large urban green spaces are environments where small mammals are abundant and human/domestic-wildlife interactions are plausible to occur. These environments are, therefore, focal points for conservation management and public health issues.The European Biodiversa BioRodDis project (https://www6.inrae.fr/biodiversa-bioroddis) aims at better understanding the relationships between small terrestrial mammal biodiversity and health in the context of global change and, in particular, of forest anthropisation and urbanisation. Here, we present the data gathered in France. The dataset will enable us to describe the diversity of small terrestrial mammal communities in forested areas corresponding to different levels of anthropisation and to evaluate the variability of this diversity over time, between seasons and years.The dataset contains occurrences of small terrestrial mammals (Rodentia and Soricomorpha) trapped in forested areas in eastern France (administrative Departments: Rhône, Ain, Jura). The sampling sites correspond to different degrees of anthropisation. Forests included in biological reserves are the least anthropised sites. Then, public forests and urban parks experience increasing levels of anthropisation. Data were collected during spring and autumn 2020 (three to four sampling sites), 2021 (six sampling sites) and 2022 (four sampling sites). These variations in the number of sites between years were due to lockdown restrictions in 2020 or to the legal authorisation to trap around biological reserves granted in 2021 only. The capture of animals was carried out in various types of forests (pine, deciduous, mixed) and in different habitats within urban parks (wooded areas, buildings, hay storage yards, riverside vegetation, restaurants, playground for kids, botanical garden, landfills). Animals were captured using live traps that were set on the ground for one to 11 nights. During this study period, 1593 small mammals were trapped and identified. They belong to 15 species, amongst which were nine species of rodents (Muridae, Cricetidae, Gliridae) and six species of shrews (Soricidae). They were weighted (gram) and measured (cm): head-body length, tail length and hind-foot length. Sexual characteristics were also recorded.
Describing patterns and testing hypotheses on processes driving biological invasions represent major issues in ecology. Addressing these questions requires building adequate data sets, i.e., covering areas and spanning periods adapted to the invasion processes studied. Rodents include major invasive species, among which the black rat Rattus rattus and the domestic mouse Mus musculus have nearly colonized the entire world, from their native Asian range. To do so, they have benefitted from their ability to cope with human-modified environments and to live in the immediate vicinity of Man, who served as a vector of their dispersal between regions and continents. In Senegal, both R. rattus and M. musculus, initially introduced by early West European colonizers some centuries ago, are currently expanding thanks to road traffic and infrastructure development and rampant urbanization that concerns even remote regions of the country. As part of projects aimed at studying (1) the role of invasive black rat populations in the emergence of zoonotic diseases in southeastern Senegal, and (2) the evolutionary consequences of parasites in R. rattus and M. musculus invasions in Senegal, we conducted a series of field campaigns throughout the southern half of the country, between May 2012 and September 2015. The objectives were to catch commensal small mammals using standard trapping procedures, identify them using morphological or molecular tools, and take samples from them upon autopsy, to look for zoonotic parasites and pathogens. Along with data on individual specimens, information on microhabitats was gathered at each trap position. This resulted in the constitution of a data set of more than 13,000 trapnights, which allowed the capture of more than 3,100 small mammals, all characterized by a series of associated biological, geographical, and environmental data. The small mammals concerned are mainly rodents (10 species), shrews, and hedgehogs. The two invasive rodent species were the most numerous, exceeding in numbers all the other species pooled. This data set makes it possible to study coarse to fine-scaled distribution of species of this commensal community in southern Senegal, as well as the possible determinants of this distribution in terms of habitat preferences and/or interspecific interactions. This data set can be freely used for non-commercial purposes and is licensed under a Creative Commons Attribution 4.0 International License.
Puumala orthohantavirus (PUUV) causes a mild form of haemorrhagic fever with renal syndrome (HFRS) called nephropathia epidemica (NE), regularly diagnosed in Europe. France represents the western frontier of the expansion of NE in Europe with two distinct areas: an endemic area (north-eastern France) where PUUV circulates in rodent populations, with the detection of many human NE cases, and a non-endemic area (south-western France) where the virus is not detected, with only a few human cases being reported. In this study, we describe the different stages of the isolation of two PUUV strains from two distinct French geographical areas: Ardennes (endemic area) and Loiret (non-endemic area). To isolate PUUV efficiently, we selected wild bank voles (Myodes glareolus, the specific reservoir of PUUV) captured in these areas and that were seronegative for anti-PUUV IgG (ELISA) but showed a non-negligible viral RNA load in their lung tissue (qRT-PCR). With this study design, we were able to cultivate and maintain these two strains in Vero E6 cells and also propagate both strains in immunologically neutral bank voles efficiently and rapidly. High-throughput and Sanger sequencing results provided a better assessment of the impact of isolation methods on viral diversity.
Sea otters, Enhydra lutris , were once abundant along the nearshore areas of the North Pacific. The international maritime fur trade that ended in 1911 left 13 small remnant populations with low genetic diversity. Subsequent translocations into previously occupied habitat resulted in several reintroduced populations along the coast of North America. We sampled sea otters between 2008 and 2011 throughout much of their current range and used 19 nuclear microsatellite markers to evaluate genetic diversity, population structure, and connectivity between remnant and reintroduced populations. Average genetic diversity within populations was similar: observed heterozygosity 0.55 and 0.53, expected heterozygosity 0.56 and 0.52, unbiased expected heterozygosity 0.57 and 0.52, for reintroduced and remnant populations, respectively. Sea otter population structure was greatest between the Northern and Southern sea otters with further structuring in Northern sea otters into Western, Central, and Southeast populations (including the reintroduced populations). Migrant analyses suggest the successful reintroductions and growth of remnant groups have enhanced connectivity and gene flow between populations throughout many of the sampled Northern populations. We recommend that future management actions for the Southern sea otter focus on future reintroductions to fill the gap between the California and Washington populations ultimately restoring gene flow to the isolated California population.
Dietary plasticity is an important issue for conservation biology as it may be essential for species to cope with environmental changes. However, this process still remains scarcely addressed in the literature, potentially because diet studies have long been constrained by methodological limits. The advent of molecular approaches now makes it possible to get a precise picture of diet and its plasticity, even for endangered and elusive species. Here we focused on the greater horseshoe bat ( Rhinolophus ferrumequinum ) in Western France, where this insectivorous species has been classified as ‘Vulnerable’ on the Regional Red List in 2016. We applied an eDNA metabarcoding approach on 1986 fecal samples collected in six maternity colonies at three sampling dates. We described its diet and investigated whether the landscape surrounding colonies and the different phases of the maternity cycle influenced the diversity and the composition of this diet. We showed that R. ferrumequinum feed on a highly more diverse spectrum of prey than expected from previous studies, therefore highlighting how eDNA metabarcoding can help improving diet knowledge of a flying elusive endangered species. Our approach also revealed that R. ferrumequinum diet is composed of two distinct features: the core diet consisting in a few preferred taxa shared by all the colonies (25% of the occurrences) and the secondary diet consisting in numerous rare prey that were highly different between colonies and sampling dates (75% of the occurrences). Energetic needs and constraints associated with the greater horseshoe bat life-cycle, as well as insect phenology and landscape features, strongly influenced the diversity and composition of both the core and whole diets. Further research should now explore the relationships between R. ferrumequinum dietary plasticity and fitness, to better assess the impact of core prey decline on R. ferrumequinum populations viability.