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Diversity, Distribution, and Drivers of Polychromophilus Infection In Diversity, distribution, and drivers of Polychromophilus infection in Malagasy bats Mercia Rasoanoro, Steven Goodman, Milijaona Randrianarivelojosia, Mbola Rakotondratsimba, Koussay Dellagi, Pablo Tortosa, Beza Ramasindrazana To cite this version: Mercia Rasoanoro, Steven Goodman, Milijaona Randrianarivelojosia, Mbola Rakotondratsimba, Kous- say Dellagi, et al.. Diversity, distribution, and drivers of Polychromophilus infection in Malagasy bats. Malaria Journal, BioMed Central, 2021, 20 (1), 10.1186/s12936-021-03696-0. hal-03200077 HAL Id: hal-03200077 https://hal.archives-ouvertes.fr/hal-03200077 Submitted on 16 Apr 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Rasoanoro et al. Malar J (2021) 20:157 https://doi.org/10.1186/s12936-021-03696-0 Malaria Journal RESEARCH Open Access Diversity, distribution, and drivers of Polychromophilus infection in Malagasy bats Mercia Rasoanoro1,2, Steven M. Goodman3,4, Milijaona Randrianarivelojosia1,5, Mbola Rakotondratsimba3, Koussay Dellagi6, Pablo Tortosa7 and Beza Ramasindrazana1,2* Abstract Background: Numerous studies have been undertaken to advance knowledge of apicomplexan parasites infecting vertebrates, including humans. Of these parasites, the genus Plasmodium has been most extensively studied because of the socio-economic and public health impacts of malaria. In non-human vertebrates, studies on malaria or malaria- like parasite groups have been conducted but information is far from complete. In Madagascar, recent studies on bat blood parasites indicate that three chiropteran families (Miniopteridae, Rhinonycteridae, and Vespertilionidae) are infected by the genus Polychromophilus with pronounced host specifcity: Miniopterus spp. (Miniopteridae) harbour Polychromophilus melanipherus and Myotis goudoti (Vespertilionidae) is infected by Polychromophilus murinus. How- ever, most of the individuals analysed in previous studies were sampled on the western and central portions of the island. The aims of this study are (1) to add new information on bat blood parasites in eastern Madagascar, and (2) to highlight biotic and abiotic variables driving prevalence across the island. Methods: Fieldworks were undertaken from 2014 to 2016 in four sites in the eastern portion of Madagascar to cap- ture bats and collect biological samples. Morphological and molecular techniques were used to identify the presence of haemosporidian parasites. Further, a MaxEnt modelling was undertaken using data from Polychromophilus mela- nipherus to identify variables infuencing the presence of this parasite Results: In total, 222 individual bats belonging to 17 species and seven families were analysed. Polychromophilus infections were identifed in two families: Miniopteridae and Vespertilionidae. Molecular data showed that Polychro- mophilus spp. parasitizing Malagasy bats form a monophyletic group composed of three distinct clades displaying marked host specifcity. In addition to P. melanipherus and P. murinus, hosted by Miniopterus spp. and Myotis goudoti, respectively, a novel Polychromophilus lineage was identifed from a single individual of Scotophilus robustus. Based on the present study and the literature, diferent biotic and abiotic factors are shown to infuence Polychromophilus infec- tion in bats, which are correlated based on MaxEnt modelling. Conclusions: The present study improves current knowledge on Polychromophilus blood parasites infecting Mala- gasy bats and confrms the existence of a novel Polychromophilus lineage in Scotophilus bats. Additional studies are needed to obtain additional material of this novel lineage to resolve its taxonomic relationship with known members of the genus. Further, the transmission mode of Polychromophilus in bats as well as its potential efect on bat popu- lations should be investigated to complement the results provided by MaxEnt modelling and eventually provide a comprehensive picture of the biology of host-parasite interactions. *Correspondence: [email protected] 2 Faculté des Sciences, Université d’Antananarivo, BP 706, Antananarivo 101, Antananarivo, Madagascar Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Rasoanoro et al. Malar J (2021) 20:157 Page 2 of 11 Keywords: Bats, Polychromophilus, Eastern, MaxEnt, Madagascar Background western dry zone [20, 21]. In terms of microorganisms In recent years, studies in diferent areas of the world hosted by Malagasy bats, diferent published studies have have elucidated the biology, ecology, diversity, and evo- demonstrated the circulation of viruses, bacteria, and lutionary history of apicomplexan parasites infecting metazoan parasites in these nocturnal mammals [22–25]. vertebrates [1–4]. Among these blood parasites, the Besides parasites of potential medical importance, bats genus Plasmodium has been the most intensively stud- from Madagascar also host malaria-related parasites, ied because of the millions of cases of malaria recorded namely the genus Polychromophilus (Haemosporida: per year, leading to more than 400,000 deaths annually in Plasmodiidae). Two species of Polychromophilus are cur- humans [5]. Plasmodium also infects diferent groups of rently documented in Malagasy bats: P. melanipherus vertebrates, such as reptiles, birds, and mammals, includ- infecting Miniopterus spp. and rarely Paratriaenops ing bats [6–8]. Te genus Plasmodium is now recognized furculus (Rhinonycteridae) and P. murinus parasitiz- to be polyphyletic and species diversifcation has led to ing Myotis goudoti (Vespertilionidae) [17, 26]. While 32 the evolution of diferent malaria or malaria-related para- species of bats occurring in the western and the central site lineages. For example, a recent study has highlighted portion of Madagascar were already screened for the that malarial parasites in general can be the subject of presence of Polychromophilus [16, 17, 26], knowledge on diferent host-switching events and shifts in life-history Polychromophilus in bats occurring in the eastern area is traits, which in turn insures their maintenance within not well-known and aspects on biotic and abiotic drivers hosts further facilitated by a simplifcation of their life of infection are far from complete. In the present study, cycle [8]. Polychromophilus diversity and distribution in bats living Based on previous observations, bats are also hosts of in the oriental portion of the island was explored and the diferent malaria-related parasites, including nine genera potential drivers of Polychromophilus infection across the of Haemoproteidae [8–15], but only four of these, includ- island predicted based on new and previous records. ing the genus Polychromophilus, are diagnosed based on molecular tools, which calls for an in-depth investigation Methods of haemosporidian parasites, including their epidemiol- Study sites ogy, host range, distribution, transmission, and patterns Fieldwork to sample bats was undertaken from 2014 to of speciation. 2016 at four main sites in eastern Madagascar: Kianjavato With respect to the genus Polychromophilus, which is Forest Station within the Paysage Harmonieux Protégé limited to bats, fve species have been formerly identi- du Corridor Forestier Ambositra-Vondrozo and sur- fed using morphological characters (Polychromophilus rounding areas; Réserve Naturelle Intégrale de Betam- adami, Polychromophilus deanei, Polychromophilus cor- pona; Parc National de Masoala; and Parc National de radetti, Polychromophilus melanipherus, and Polychro- Marojejy (Fig. 1, Additional fle 1: Table S1). A range of mophilus murinus) of which two have been molecularly habitat types were investigated, including day roosts in characterized (P. melanipherus and P. murinus) infect- buildings, degraded areas associated with croplands, and ing Miniopteridae [16, 17] and Vespertilionidae [17, 18], lowland moist evergreen forests. respectively. Further molecular research has revealed
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