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Phylogeny of Hepatocystis Parasites of Australian Flying Foxes

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Phylogeny of Hepatocystis Parasites of Australian Flying Foxes View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Queensland DAF eResearch Archive IJP: Parasites and Wildlife 7 (2018) 207–212 Contents lists available at ScienceDirect IJP: Parasites and Wildlife journal homepage: www.elsevier.com/locate/ijppaw Phylogeny of Hepatocystis parasites of Australian flying foxes reveals distinct ☆ T parasite clade ∗ Juliane Schaera,b, , Lee McMichaelc, Anita N. Gordond, Daniel Russella, Kai Matuschewskib, Susan L. Perkinse, Hume Fieldf, Michelle Powera a Department of Biological Sciences, Macquarie University, North Ryde, 2109, Australia b Department of Molecular Parasitology, Institute of Biology, Humboldt University, 10117, Berlin, Germany c School of Veterinary Science, University of Queensland, Gatton Campus, Gatton, QLD, 4343, Australia d Biosecurity Sciences Laboratory, Health and Food Science Precinct, 39 Kessels Rd, Coopers Plains, Queensland, 4108, Australia e Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY, 10024, USA f EcoHealth Alliance, New York, NY, 10001, USA ARTICLE INFO ABSTRACT Keywords: Hepatocystis parasites are close relatives of mammalian Plasmodium species and infect a range of primates and Haemosporida bats. Here, we present the phylogenetic relationships of Hepatocystis parasites of three Australian flying fox Hepatocystis species. Multilocus phylogenetic analysis revealed that Hepatocystis parasites of Pteropus species from Australia Chiroptera and Asia form a distinct clade that is sister to all other Hepatocystis parasites of primates and bats from Africa and Malaria Asia. No patterns of host specificity were recovered within the Pteropus-specific parasite clade and the Pteropus Hepatocystis sequences from all three Australian host species sampled fell into two divergent clades. Australia 1. Introduction other haemosporidian parasite genera. Bats (Chiroptera) are hosts to perhaps the most diverse array of The life-threatening disease malaria is caused by single-cell eu- haemosporidian parasites among mammals, with nine different genera karyotic parasites of the genus Plasmodium. The human-infecting described in this mammalian order. The parasite genera in bats com- Plasmodium species belong to a large monophyletic group of haemos- prise species of Plasmodium and Hepatocystis, and seven genera thought poridian parasites (Haemosporida) that comprise 200 formally de- to exclusively infect chiropteran hosts (Perkins and Schaer, 2016). Due scribed species of Plasmodium and almost 300 closely related species to this diversity, bat malaria parasites are of particular interest for the (Martinsen and Perkins, 2013; Galen et al., 2018). These parasites infect study of the taxonomy and systematics of malaria parasites. Recent a diverse array of dipteran invertebrate as well as vertebrate hosts. molecular studies have mainly focused on bat malaria parasites from Mammalian haemosporidian parasites are currently classified in ten African and European bat hosts (e.g. Witsenburg et al., 2012; Schaer different genera, including Plasmodium and Hepatocystis, whereas the et al., 2013; Lutz et al., 2016; Schaer et al., 2017). In contrast, our mammalian Plasmodium clade is paraphyletic, because it contains the knowledge of haemosporidian parasites of Australian bats is very lim- parasites of the genus Hepatocystis (Perkins and Schaer, 2016; Galen ited and restricted to morphological investigations, with no molecular et al., 2018). The large group of haemosporidian parasites not only data available for any of the haemosporidian parasites in these bats. differs in host preferences, but also in morphology, life history and Molecular studies have greatly improved our understanding of hae- effects on their hosts. Uncovering the evolutionary history and biology mosporidian parasites. They are particularly needed for the character- of these parasites will help define their biological adaptations, host ization of the understudied haemosporidians of wildlife to recover the switches and acquisitions of novel life-history traits. For example, er- evolutionary history of key life-history characters of the whole group, ythrocytic schizogony or the multiplication of parasites in the blood, to determine host specificity patterns and the transitions among the the life cycle stage that is associated with the characteristic clinical different dipteran and vertebrate host groups (Martinsen and Perkins, signs of malaria in humans, is exclusive to parasites of the genus Plas- 2013). Further, molecular identifications allow the differentiation of modium (that infect several groups of vertebrates) and is absent in all parasites that are morphologically indistinguishable and are essential ☆ Note: Nucleotide sequence data reported in this paper are available in the GenBank database under accession nos. MH397732-MH397876. ∗ Corresponding author. Department of Biological Sciences, Macquarie University, North Ryde, 2109, Australia. E-mail address: [email protected] (J. Schaer). https://doi.org/10.1016/j.ijppaw.2018.06.001 Received 2 May 2018; Received in revised form 31 May 2018; Accepted 5 June 2018 2213-2244/ © 2018 The Authors. Published by Elsevier Ltd on behalf of Australian Society for Parasitology. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). J. Schaer et al. IJP: Parasites and Wildlife 7 (2018) 207–212 for any taxonomic revisions of described morphospecies (Galen et al., Table 1 2018). Based on morphological criteria, four haemosporidian genera List of investigated samples and corresponding blood stage morphology. have been reported in Australian bat hosts: Hepatocystis, Poly- aSample/Abbreviation in Locality bblood stage morphology chromophilus, Johnsprentia and Sprattiella (Table S1). The conception of phylogenetic trees the two genera Johnsprentia and Sprattiella has only been introduced very recently (Landau et al., 2012a, b). The parasite observations that P_alecto_A17 Ayr No blood smear available P_alecto_A22 Tallebudgera No blood smear available led to the description of these two new parasite genera were gathered P_alecto_L1 Boonah Category 2 from infected Pteropus alecto individuals collected in Townsville, P_alecto_L2 Boonah Subpatent infection, no Queensland, Australia in 1978. Both Johnsprentia and Sprattiella await parasites detected independent confirmation. Polychromophilus parasites only infect in- P_alecto_L3 Boonah Category 2 sectivorous bats of the bat families Miniopteridae and Vespertilionidae P_alecto_L5 Boonah Category 2 P_alecto_L7 Boonah No blood smear available (suborder Yangochiroptera) and display a wide distribution in tempe- P_alecto_L8 Boonah Category 2 rate and tropical areas worldwide. In contrast, Hepatocystis is restricted P_alecto_L10 Boonah No blood smear available to two bat families of the suborder Yinpterochiroptera, fruit bat/flying P_alecto_L11 Boonah No blood smear available fox species (Pteropodidae) and hipposiderid bats (Hipposideridae) of P_alecto_L13 Boonah No blood smear available fi P_conspicillatus_A25 Topaz No blood smear available Africa, Asia and Australia (c.f. Perkins and Schaer, 2016). The rst re- P_conspicillatus_L14 Gordonvale Category 1 ports of Hepatocystis in Australian flying foxes date back to 1909 and P_conspicillatus_L15 Gordonvale Category 1 1911, with “Plasmodium” infections independently reported in Pteropus P_conspicillatus_L16 Gordonvale Category 1 alecto gouldi (Breinl et al., 1912). The parasite species was originally P_conspicillatus_L17 Gordonvale Category 1 described as Plasmodium pteropi, and later reclassified as Hepatocystis P_conspicillatus_L18 Gordonvale Category 1 fl P_conspicillatus_L19 Gordonvale Category 1 pteropi (Manwell, 1946; Garnham, 1966). Four Australian ying fox P_conspicillatus_L20 Gordonvale Category 1 species of the genus Pteropus (Pteropus alecto, Pteropus poliocephalus, P_conspicillatus_L21 Gordonvale Category 1 Pteropus scapulatus, Pteropus conspicillatus) were subsequently identified P_conspicillatus_L22 Gordonvale No blood smear available as hosts for H. pteropi (Mackerras, 1959). A second species of Hepato- P_conspicillatus_L23 Gordonvale No blood smear available P_conspicillatus_L25 Gordonvale No blood smear available cystis, Hepatocystis levinei was described from P. poliocephalus (Landau P_conspicillatus_L27 Gordonvale No blood smear available et al., 1985) and more recently, a study reported the same species from P_conspicillatus_L32 Gordonvale No blood smear available P. alecto, sampled in Queensland in 1978 (Landau et al., 2012a). P_conspicillatus_L33 Gordonvale No blood smear available Mammalian haemosporidian genera that lack asexual replication in the P_conspicillatus_L34 Gordonvale No blood smear available blood (all haemosporidian genera except Plasmodium) are generally P_conspicillatus_L35 Gordonvale No blood smear available P_conspicillatus_L37 Gordonvale Category 2 considered as benign infections in their mammalian hosts. The blood P_conspicillatus_L40 Gordonvale Category 2 stages of Hepatocystis, Sprattiella and Johnsprentia parasites are confined P_conspicillatus_L41 Gordonvale No blood smear available to gametocytes, whereas the schizonts occur in different tissues. Ac- P_conspicillatus_L43 Gordonvale Category 1 cording to the authors, Sprattiella-infected bats feature schizonts in the P_scapulatus_A1 North Lakes No blood smear available P_scapulatus_A2 Caboolture No blood smear available lumen of renal veins of the kidney and Johnsprentia parasites develop
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