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Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin

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Abstract

Species of Hepatozoon Miller, 1908 are blood parasites most commonly found in snakes but some have been described from all tetrapod groups and a wide variety of hematophagous invertebrates. Previous studies have suggested possible associations between Hepatozoon spp. found in predators and prey. Particularly, some saurophagous snakes from North Africa and the Mediterranean region have been found to be infected with Hepatozoon spp. similar to those of various sympatric lizard hosts. In this study, we have screened tissue samples of 111 North African and Mediterranean snakes, using specific primers for the 18S rRNA gene. In the phylogenetic analysis, the newly-generated Hepatozoon spp. sequences grouped separately into five main clusters. Three of these clusters were composed by Hepatozoon spp. also found in snakes and other reptiles from the Mediterranean Basin and North Africa. In the other two clusters, the new sequences were not closely related to geographically proximate known sequences. The phylogeny of Hepatozoon spp. inferred here was not associated with intermediate host taxonomy or geographical distribution. From the other factors that could explain these evolutionary patterns, the most likely seems series of intermediate hosts providing similar ribotypes of Hepatozoon and a high prevalence of host shifts for Hepatozoon spp. This is indicated by ribotypes of high similarity found in different reptile families, as well as by divergent ribotypes found in the same host species. This potentially low host specificity has profound implications for the systematics of Hepatozoon spp.

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Acknowledgements

Sampling in Turkey and the Caucasus was supported by the project “Preserving Armenian biodiversity: Joint Portuguese – Armenian program for training in modern conservation biology” funded by Gulbenkian Foundation. Sampling in North-West Africa was partially supported by the National Geographic Society (CRE-7629-04, CRE-8412-08) and by Fundação para a Ciência e Tecnologia (FCT: PTDC/BIA-BEC/099934/2008) through the EU Programme COMPETE, and by the Percy Sladen fund. JPM is supported by a Fundação para a Ciência e a Tecnologia (FCT) PhD grant (SFRH/BD/74305/2010) and co-financed by FSE and POPH and EU. DJH and JCB are supported by “Genomics and evolutionary biology” and “Biodiversity, Ecology and Global Change”, respectively, co-financed by the North Portugal Regional Operational Programme 2007/2013 (ON.2 - O Novo Norte), under the National Strategic Reference Framework (NSRF), through the European Regional Development Fund (ERDF). Snakes were captured and handled under permits from the Italian Ministry of the Environment (DPN/2D/2003/2267). DS is supported by a FCT post-doctoral fellowship SFRH/BPD/66592/2009 and AP by a FCT IF contract IF/01257/2012. We thank Cristiano Liuzzi and the many students and colleagues who helped during fieldwork.

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Tomé, B., Maia, J.P., Salvi, D. et al. Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin. Syst Parasitol 87, 249–258 (2014). https://doi.org/10.1007/s11230-014-9477-4

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