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      Leishmania major and Trypanosoma lewisi infection in invasive and native rodents in Senegal

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          Abstract

          Bioinvasion is a major public health issue because it can lead to the introduction of pathogens in new areas and favours the emergence of zoonotic diseases. Rodents are prominent invasive species, and act as reservoirs in many zoonotic infectious diseases. The aim of this study was to determine the link between the distribution and spread of two parasite taxa ( Leishmania spp. and Trypanosoma lewisi) and the progressive invasion of Senegal by two commensal rodent species (the house mouse Mus musculus domesticus and the black rat Rattus rattus). M. m. domesticus and R. rattus have invaded the northern part and the central/southern part of the country, respectively. Native and invasive rodents were caught in villages and cities along the invasion gradients of both invaders, from coastal localities towards the interior of the land. Molecular diagnosis of the two trypanosomatid infections was performed using spleen specimens. In the north, neither M. m. domesticus nor the native species were carriers of these parasites. Conversely, in the south, 17.5% of R. rattus were infected by L. major and 27.8% by T. lewisi, while very few commensal native rodents were carriers. Prevalence pattern along invasion gradients, together with the knowledge on the geographical distribution of the parasites, suggested that the presence of the two parasites in R. rattus in Senegal is of different origins. Indeed, the invader R. rattus could have been locally infected by the native parasite L. major. Conversely, it could have introduced the exotic parasite T. lewisi in Senegal, the latter appearing to be poorly transmitted to native rodents. Altogether, these data show that R. rattus is a carrier of both parasites and could be responsible for the emergence of new foci of cutaneous leishmaniasis, or for the transmission of atypical human trypanosomiasis in Senegal.

          Author summary

          Biological invasions (the introduction and adaptation of living organisms to a new environment) are increasingly frequent due to worldwide intensification of human-associated exchanges. They can lead to the introduction of pathogens in new areas and favour the emergence of diseases. Rodents are prominent invasive species, and act as reservoirs in many infectious diseases. The aim of our study was to determine the link between the distribution and spread of two parasites, Leishmania spp. and Trypanosoma lewisi, and the progressive invasion of Senegal by two commensal rodent species, the house mouse Mus musculus domesticus, and the black rat Rattus rattus. We identified R. rattus as a potential reservoir for Leishmania major and T. lewisi in the southern part of Senegal. The presence of these two pathogens in R. rattus may be of different origins. The invader R. rattus could have been locally contaminated with L. major. Conversely, T. lewisi infection could have been introduced in Senegal by R. rattus, and seems to be poorly transmitted to native rodents. Altogether, these data show that R. rattus is a carrier of both parasites, and could be responsible for the emergence of new foci of cutaneous leishmaniasis or for the transmission of atypical human trypanosomiasis in Senegal.

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          Most cited references101

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          A Historical Overview of the Classification, Evolution, and Dispersion of Leishmania Parasites and Sandflies

          Background The aim of this study is to describe the major evolutionary historical events among Leishmania, sandflies, and the associated animal reservoirs in detail, in accordance with the geographical evolution of the Earth, which has not been previously discussed on a large scale. Methodology and Principal Findings Leishmania and sandfly classification has always been a controversial matter, and the increasing number of species currently described further complicates this issue. Despite several hypotheses on the origin, evolution, and distribution of Leishmania and sandflies in the Old and New World, no consistent agreement exists regarding dissemination of the actors that play roles in leishmaniasis. For this purpose, we present here three centuries of research on sandflies and Leishmania descriptions, as well as a complete description of Leishmania and sandfly fossils and the emergence date of each Leishmania and sandfly group during different geographical periods, from 550 million years ago until now. We discuss critically the different approaches that were used for Leishmana and sandfly classification and their synonymies, proposing an updated classification for each species of Leishmania and sandfly. We update information on the current distribution and dispersion of different species of Leishmania (53), sandflies (more than 800 at genus or subgenus level), and animal reservoirs in each of the following geographical ecozones: Palearctic, Nearctic, Neotropic, Afrotropical, Oriental, Malagasy, and Australian. We propose an updated list of the potential and proven sandfly vectors for each Leishmania species in the Old and New World. Finally, we address a classical question about digenetic Leishmania evolution: which was the first host, a vertebrate or an invertebrate? Conclusions and Significance We propose an updated view of events that have played important roles in the geographical dispersion of sandflies, in relation to both the Leishmania species they transmit and the animal reservoirs of the parasites.
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            Terrestrial ecosystem responses to species gains and losses.

            Ecosystems worldwide are losing some species and gaining others, resulting in an interchange of species that is having profound impacts on how these ecosystems function. However, research on the effects of species gains and losses has developed largely independently of one another. Recent conceptual advances regarding effects of species gain have arisen from studies that have unraveled the mechanistic basis of how invading species with novel traits alter biotic interactions and ecosystem processes. In contrast, studies on traits associated with species loss are fewer, and much remains unknown about how traits that predispose species to extinction affect ecological processes. Species gains and losses are both consequences and drivers of global change; thus, explicit integration of research on how both processes simultaneously affect ecosystem functioning is key to determining the response of the Earth system to current and future human activities.
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              2000 Report of the AVMA Panel on Euthanasia.

              (2001)
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                Author and article information

                Contributors
                Role: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Formal analysisRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                29 June 2018
                June 2018
                : 12
                : 6
                : e0006615
                Affiliations
                [1 ] MIVEGEC, IRD, CNRS, Univ. Montpellier, Montpellier, France
                [2 ] CBGP, IRD, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier, Montpellier, France
                [3 ] CBGP, IRD, CIRAD, INRA, Montpellier SupAgro, Univ Montpellier, Campus ISRA/IRD de Bel Air, Dakar, Sénégal
                [4 ] Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop (UCAD), Dakar, Sénégal
                [5 ] CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ Montpellier, Montpellier, France
                [6 ] IRD, LPED (UMR AMU/IRD), Marseille, France
                Universiteit Antwerpen, BELGIUM
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2205-8222
                http://orcid.org/0000-0002-6406-1270
                http://orcid.org/0000-0002-5075-4121
                Article
                PNTD-D-18-00248
                10.1371/journal.pntd.0006615
                6042788
                29958273
                2c9c45b9-c101-4f8a-988a-fb63198c766b
                © 2018 Cassan et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 February 2018
                : 17 June 2018
                Page count
                Figures: 2, Tables: 2, Pages: 21
                Funding
                Funded by: Institut de Recherche pour le Développement (FR)
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-11-JSV7-0006
                Award Recipient :
                The authors received a funding from the Agence NAtionale pour la Recherche (ANR "ENEMI", ANR-11-JSV7-0006) [CB, ALB]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Rodents
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Trypanosoma
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Leishmania
                People and Places
                Geographical Locations
                Africa
                Senegal
                Medicine and Health Sciences
                Parasitic Diseases
                Ecology and Environmental Sciences
                Species Colonization
                Invasive Species
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-07-12
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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