Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar

Parasite, Sep 2014

Madagascar is one of the world’s top twelve “megadiversity” hot spots hosting unique and threatened flora and fauna. Parasites are a major component of biodiversity but remain largely uncharacterized in wildlife. In this study we combine microscopic and molecular assessment of hemoparasites in endemic reptile species from Madagascar. We detected three distinct parasites: the apicomplexans Hepatozoon and Sarcocystis, and filarial nematodes. The prevalence and intensity of these apicomplexans were low overall, while microfilarial infections in chameleons were relatively high. We detected mixed infections of two Hepatozoon haplotypes in Madagascarophis colubrinus, and of Hepatozoon and microfilariae in a Furcifer sp. Phylogenetic analyses of Hepatozoon showed evidence of prey-predator transmission, with identical sequences found in the snakes M. colubrinus and Ithycyphus oursi, and their prey Furcifer sp. Based on previous studies regarding the life cycle of Hepatozoon domerguei Landau, Chabaud, Michel, and Brygoo, 1970 in these hosts and due to their morphological similarity, we propose that this Hepatozoon haplotype is Hepatozoon domerguei. Future studies, including the examination of invertebrate hosts, are needed to verify this preliminary taxonomic identification. A distinct hemogregarine haplotype was found in Oplurus sp., which displayed morphologically different gametocytes, some of which were apparently inside leukocytes. The Sarcocystis identified from Tracheloptychus petersi was identical to that reported in a North African snake, indicating that the same lineage is found in geographically distinct regions. By combining morphological and genetic information, Foleyella furcata (Linstow, 1899) filarial nematodes were identified in several Furcifer chameleons. This study provides insights into the distribution, diversity and host-parasite interactions of hemoparasites in wild reptile populations from Madagascar.Madagascar est l’un des douze premiers points chauds de « mégadiversité » au monde et héberge une flore et une faune exceptionnelles et menacées. Les parasites sont une composante majeure de la biodiversité, mais restent largement non caractérisés dans la faune sauvage. Dans cette étude, nous combinons des évaluations microscopiques et moléculaires des hémoparasites chez des espèces de reptiles endémiques de Madagascar. Nous avons détecté trois parasites distincts : les apicomplexes Hepatozoon et Sarcocystis, et des nématodes filaires. La prévalence et l’intensité de ces apicomplexes étaient globalement faibles, tandis que les infections de microfilaires chez les caméléons étaient relativement élevées. Nous avons détecté des infections mixtes de deux haplotypes d’Hepatozoon chez Madagascarophis colubrinus, et d’Hepatozoon et de microfilaires chez Furcifer sp. Les analyses phylogénétiques d’Hepatozoon montraient des signes de transmission proie-prédateur avec des séquences identiques trouvés chez les serpents M. colubrinus et Ithycyphus oursi, et leurs proies Furcifer sp. Sur la base d’études antérieures concernant le cycle de vie de Hepatozoon domerguei Landau, Chabaud, Michel et Brygoo, 1970 chez ces hôtes et en raison de leur similitude morphologique, nous proposons que cet haplotype d’Hepatozoon est Hepatozoon domerguei. Les études futures, y compris l’examen des hôtes invertébrés sont nécessaires pour vérifier cette identification taxonomique préliminaire. On a trouvé chez Oplurus sp. un haplotype distinct d’hémogrégarine qui montre des gamétocytes morphologiquement différents, dont certains étaient apparemment à l’intérieur des leucocytes. Le Sarcocystis identifié chez Tracheloptychus petersi était identique à celui rapporté dans un serpent d’Afrique du Nord, ce qui indique que la même lignée se trouve dans des régions géographiquement distinctes. En combinant information morphologique et génétique, le nématode filaire Foleyella furcata (Linstow, 1899) a été identifié chez plusieurs caméléons du genre Furcifer. Cette étude donne un aperçu sur la répartition, la diversité et les interactions hôtes-parasites des hémoparasites dans les populations de reptiles sauvages de Madagascar.

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Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar

Parasite Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar Joa˜o P. Maia 0 1 2 Angelica Crottini 2 David James Harris 1 2 0 Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra) , Passeig Mar ́ıtim de la Barceloneta 37-49, 08003 Barcelona , Spain 1 Departamento de Biologia, Faculdade de Cieˆncias, Universidade do Porto , Rua do Campo Alegre FC4, 4169-007 Porto , Portugal 2 CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto , Campus Agra ́rio de Vaira ̃o, Rua Padre Armando Quintas, N 7, 4485-661 Vaira ̃o, Vila do Conde , Portugal - Madagascar is one of the world's top twelve ''megadiversity'' hot spots hosting unique and threatened flora and fauna. Parasites are a major component of biodiversity but remain largely uncharacterized in wildlife. In this study we combine microscopic and molecular assessment of hemoparasites in endemic reptile species from Madagascar. We detected three distinct parasites: the apicomplexans Hepatozoon and Sarcocystis, and filarial nematodes. The prevalence and intensity of these apicomplexans were low overall, while microfilarial infections in chameleons were relatively high. We detected mixed infections of two Hepatozoon haplotypes in Madagascarophis colubrinus, and of Hepatozoon and microfilariae in a Furcifer sp. Phylogenetic analyses of Hepatozoon showed evidence of prey-predator transmission, with identical sequences found in the snakes M. colubrinus and Ithycyphus oursi, and their prey Furcifer sp. Based on previous studies regarding the life cycle of Hepatozoon domerguei Landau, Chabaud, Michel, and Brygoo, 1970 in these hosts and due to their morphological similarity, we propose that this Hepatozoon haplotype is Hepatozoon domerguei. Future studies, including the examination of invertebrate hosts, are needed to verify this preliminary taxonomic identification. A distinct hemogregarine haplotype was found in Oplurus sp., which displayed morphologically different gametocytes, some of which were apparently inside leukocytes. The Sarcocystis identified from Tracheloptychus petersi was identical to that reported in a North African snake, indicating that the same lineage is found in geographically distinct regions. By combining morphological and genetic information, Foleyella furcata (Linstow, 1899) filarial nematodes were identified in several Furcifer chameleons. This study provides insights into the distribution, diversity and host-parasite interactions of hemoparasites in wild reptile populations from Madagascar. Hemogregarine; Sarcocystis; Apicomplexa; Nematode; Filaria; Arthropod-borne diseases - distinct d’he´mogre´garine qui montre des game´tocytes morphologiquement diffe´rents, dont certains e´taient apparemment a` l’inte´rieur des leucocytes. Le Sarcocystis identifie´ chez Tracheloptychus petersi e´tait identique a` celui rapporte´ dans un serpent d’Afrique du Nord, ce qui indique que la meˆme ligne´e se trouve dans des re´gions ge´ographiquement distinctes. En combinant information morphologique et ge´ne´tique, le ne´matode filaire Foleyella furcata (Linstow, 1899) a e´te´ identifie´ chez plusieurs came´le´ons du genre Furcifer. Cette e´tude donne un aperc¸u sur la re´partition, la diversite´ et les interactions hoˆtes-parasites des he´moparasites dans les populations de reptiles sauvages de Madagascar. Introduction Madagascar is the fourth largest island in the world, and as one of the world’s top 12 ‘‘megadiversity’’ hot spots [ 54 ] hosts an almost unparalleled concentration of endemic, diverse and threatened fauna and flora [ 54, 88 ]. The native reptile fauna has a high level of endemism at the species level (about 92%), and is composed of at least 25 extant independent lineages [ 17, 24 ]. Currently, more than 400 reptile species are known in Madagascar [ 56 ], and this list will increase in the future as a result of intense research activities and widespread application of integrative taxonomic approaches [ 24, 56 ], as shown by the numerous recent species descriptions [ 18, 25, 69 ]. Parasites have been increasingly recognized as a main component of biodiversity; however, their study clearly lags behind that of their hosts [53]. Documenting the diversity of parasites is important for several reasons, since they (1) coevolve and interact with their hosts [ 59, 75 ], (2) play an important role in structuring animal communities [ 31, 65 ], and (3) are important in ecosystems and conservation [ 61, 72 ]. Hemoparasites typically have complex life cycles, requiring more than one host to complete it. The life cycle of several filarial and coccidian parasites has been described in endemic hosts from Madagascar: Foleyella furcata (Linstow, 1899) [ 44 ], an onchocercid described from the chameleon Furcifer verrucosus (Cuvier, 1829) [ 7 ], and Hepatozoon domerguei (Landau, Chabaud, Michel (...truncated)


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João P. Maia, Angelica Crottini, David James Harris. Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar, Parasite, 2014, pp. 47, 21, DOI: 10.1051/parasite/2014046