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Experimental and Applied Acarology

, Volume 73, Issue 3–4, pp 501–519 | Cite as

Distribution and phylogeny of Hyalomma ticks (Acari: Ixodidae) in Turkey

  • Olcay Hekimoglu
  • Ayşe Nurdan Ozer
Article

Abstract

The genus Hyalomma includes some of the most medically and veterinarily important tick species in the world. To clarify and identify the current distribution of the species of Hyalomma, field studies were conducted in 65 localities in Turkey and five localities in Cyprus. Additionally, using mitochondrial 12S and 16S ribosomal DNA, specimens of Hyalomma from Turkey, H. excavatum from Cyprus, H. marginatum from Spain and Italy were evaluated together with the available sequences obtained from Genbank. Morphological and molecular analyses demonstrated the presence of four species in Turkey: H. marginatum, H. excavatum, H. aegyptium and H. asiaticum. Hyalomma marginatum is the dominant species in the Central and Northern parts of Turkey, whereas H. excavatum distributes mostly in the Southern parts. Hyalomma asiaticum is restricted to the Southeastern Anatolia. However, some sympatric regions were observed for these species. Phylogenetic trees obtained with Maximum Likelihood method demonstrated five clades. Data supported previous conclusions, but placed H. asiaticum, H. scupense, H. dromedarii and H. aegyptium in different clades with high bootstrap values. Specimens of H. anatolicum group and H. marginatum complex are sister groups. Pairwise distance analyses of these groups showed 2.8 and 3% differences for 12S rDNA and 16S rDNA, respectively. Therefore, additional analyses with the samples from different locations using different markers need to evaluate the exact status of the species of these groups.

Keywords

Hyalomma Hyalomma marginatum Distribution Phylogeny Turkey 12S rDNA 16S rDNA 

Notes

Acknowledgements

This work was supported by the Hacettepe University Research Fund (Grant Nos. FUA-2015-5895 and FDK-2016-11293). Many thanks to Prof. Dr. Lorenza Beati that we conducted the molecular part of this work in US National Tick Collection, Georgia Southern University, Statesboro. We are also grateful to Agustin Estrada-Pena (University of Zaragoza, Spain) for his help on the morphological identification and for providing us H. marginatum samples from Spain and Italy. Special thanks to Dr. Arda Cem Kuyucu and Dr. Ismail Kudret Sağlam for critical reading of the manuscript and Salim Calis for technical assistance during the field studies.

Supplementary material

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Supplementary material 1 (DOCX 19 kb)

References

  1. Apanaskevich D, Horak I (2005) The genus Hyalomma Koch, 1844. II. Taxonomic status of H. (Euhyalomma) anatolicum Koch, 1844, H. (E.) excavatum Koch, 1844 (Acari, Ixodidae) with redescriptions of all stages. Acarina 13:181–197Google Scholar
  2. Apanaskevich DA, Horak IG (2008) The genus Hyalomma Koch, 1844: V. Re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species (Acari: Ixodidae) with redescription of all parasitic stages and notes on biology. Int J Acarol 34:13–42.  https://doi.org/10.1080/01647950808683704 CrossRefGoogle Scholar
  3. Apanaskevich D, Horak I (2010) The genus Hyalomma. XI. Redescription of all parasitic stages of H. (Euhyalomma) asiaticum (Acari: Ixodidae) and notes on its biology. Exp Appl Acarol 52:207–220.  https://doi.org/10.1007/s10493-010-9361-0 CrossRefPubMedGoogle Scholar
  4. Apanaskevich DA, Filippova NA, Horak IG (2010) The genus Hyalomma Koch, 1844. X. Redescription of all parasitic stages of H. (Euhyalomma) scupense Schulze, 1919 (= H. detritum schulze) (Acari: Ixodidae) and notes on its biology. Folia Parasitol 57(1):69–78CrossRefPubMedGoogle Scholar
  5. Araya-Anchetta A (2012) A study of macro and micro-evolutionary factors determining population genetics in ticks. Dissertation, Northern Arizona University, FlagstaffGoogle Scholar
  6. Araya-Anchetta A, Scoles G, Giles J, Busch J, Wagner D (2013) Hybridization in natural sympatric populations of Dermacentor ticks in northwestern North America. Ecol Evol 3:714–724CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bakheit MA, Latif AA, Vatansever Z, Seitzer U, Ahmed J (2012) The huge risks due to Hyalomma ticks arthropods as vectors of emerging diseases. Springer, Berlin, pp 167–194CrossRefGoogle Scholar
  8. Barker SC, Murrell A (2003) Phylogeny, evolution and historical zoogeography of ticks: a review of recent progress ticks and tick-borne pathogens. Springer, Berlin, pp 55–68CrossRefGoogle Scholar
  9. Barker S, Murrell A (2004) Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129:S15–S36CrossRefPubMedGoogle Scholar
  10. Baziz-Neffah F, Bitam I, Kernif T, Beneldjouzi A, Boutellis A, Berenger JM, Zenia S, Doumandji S (2015) Contribution a la Connaissance des Ectoparasites d’oiseaux en Algerie. Bull Soc Zool Fr 140(2):81–98Google Scholar
  11. Beati L, Keirans JE (2001) Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12s ribosomal DNA gene sequences and morphological characters. J Parasitol 87:32–48CrossRefPubMedGoogle Scholar
  12. Beati L, Patel J, Lucas-Williams H et al (2012) Phylogeography and demographic history of Amblyomma variegatum (fabricius) (Acari: Ixodidae), the tropical bont tick. Vector Borne Zoonotic Dis 12:514–525CrossRefPubMedPubMedCentralGoogle Scholar
  13. Black WC, Piesman J (1994) Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16s rdna sequences. Proc Natl Acad Sci 91:10034–10038CrossRefPubMedPubMedCentralGoogle Scholar
  14. Black WC, Klompen J, Keirans JE (1997) Phylogenetic relationships among tick subfamilies (Ixodida: Ixodidae: Argasidae) based on the 18s nuclear rDNA gene. Mol Phylogenet Evol 7:129–144CrossRefPubMedGoogle Scholar
  15. Bursali A, Keskin A, Tekin S (2012) A review of the ticks (Acari: Ixodida) of Turkey: species diversity, hosts and geographical distribution. Exp Appl Acarol 57:91–104.  https://doi.org/10.1007/s10493-012-9530-4 CrossRefPubMedGoogle Scholar
  16. Camicas JL, Hervy JP, Adam F, Morel PC (1998) The ticks of the world (Acarida, Ixodida): nomenclature, described stages, hosts, distribution, ParisGoogle Scholar
  17. Casati S, Bernasconi MV, Gern L, Piffaretti JC (2008) Assessment of intraspecific mtdna variability of european Ixodes ricinus sensu stricto (Acari: Ixodidae). Infect Genet Evol 8:152–158CrossRefPubMedGoogle Scholar
  18. Chitimia-Dobler L, Nava S, Bestehorn M, Dobier G, Wölfel S (2016) First detection of Hyalomma rufipes in Germany. Ticks Tick-borne Dis 7:1135–1138CrossRefPubMedGoogle Scholar
  19. Chisu V, Zobba R, Foxi C, Pisu D, Masala G, Alberti A (2016) Molecular detection and groEL typing of Rickettsia aeschlimannii in Sardinian tick. Parasitol Res 115(9):3323–3328CrossRefPubMedGoogle Scholar
  20. Chochlakis D, Ioannou I, Sandalakis V, Dimitriou T, Kassinis N, Papadopoulos B, Tselentis Y, Psaroulaki A (2012) Spotted fever group rickettsiae in ticks in Cyprus. Microb Ecol 63:314–323CrossRefPubMedGoogle Scholar
  21. Delpy LP (1947) Révision, par des voies expérimentales, du genre Hyalomma C.L., Koch 1884 (Acarina, Ixodoidea, Ixodidae). Note préliminaire. Ann Parasitol Hum Comp 21:267–293CrossRefGoogle Scholar
  22. Dohm DJ, Logan TM, Linthicum KJ, Rossi CA, Turell MJ (1996) Transmission of Crimean-Congo hemorrhagic fever virus by Hyalomma impeltatum (Acari: Ixodidae) after experimental infection. J Med Entomol 33:848–851CrossRefPubMedGoogle Scholar
  23. Epis S, Sassera D, Beninati T, Lo N, Beati L, Piesman J, Rinaldi L, McCoy KD, Torina A, Sacchi L, Clementi E, Genchi M, Magnino S, Bandi C (2008) Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology 135(4):485–494CrossRefPubMedGoogle Scholar
  24. Erster O, Roth A, Akkad F, Zonstein I, King R, Orshan L (2015) Parasitology. Kimorn Veterinary Institute, Bet DaganGoogle Scholar
  25. Estrada-Peña A, Bouattour A, Camicas J, Walker A (2004) Ticks of domesfic animals in mediterranean region, a guide to idenfificafion of species. Univerity of Zaragoza, ZaragozaGoogle Scholar
  26. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefPubMedGoogle Scholar
  27. Gou H, Guan G, Liu A et al (2013) Coevolutionary analyses of the relationships between piroplasmids and their hard tick hosts. Ecol Evol 3:2985–2993CrossRefPubMedPubMedCentralGoogle Scholar
  28. Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG, Shao R, Barker S (2010) The argasidae, ixodidae and nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa 2528:1–28Google Scholar
  29. Guglielmone AA, Nava S, Mastropaolo M, Mangold AJ (2013) Distribution and genetic variation of Amblyomma triste (Acari: Ixodidae) in Argentina. Ticks Tick Borne Dis 4:386–390CrossRefPubMedGoogle Scholar
  30. Hekimoğlu O, Sağlam İK, Özer N, Estrada-Peña A (2016) New molecular data shed light on the global phylogeny and species limits of the Rhipicephalus sanguineus complex. Ticks Tick Borne Dis 7:798–807CrossRefPubMedGoogle Scholar
  31. Hewitt GM, Johnston AW, Young JPW (2013) Molecular techniques in taxonomy, vol 57. Springer, BerlinGoogle Scholar
  32. Hoogstraal H (1956) African ixodoidea Voi I Ticks of the Sudan (with special reference to Equatoria province and with preliminary reviews of the genera Boophilus, Margaropus, and Hyalomma). African Ixodoidea Department of the Navy, Bureau of Medicine and Surgery, WashingtonGoogle Scholar
  33. Hoogstraal H (1979) Review article: the epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J Med Entomol 15:307–417CrossRefPubMedGoogle Scholar
  34. Hoogstraal H, Aeschlimann A (1982) Tick-host specificity (Ixodoidae, vertebrates). Memoires du Museum National d’Histoire Naturelle Serie A Zoologie (France)Google Scholar
  35. Hoogstraal H, Kaiser MN, Traylor MA, Guindy E, Gaber S (1961) Ticks (Ixodidae) on birds migrating from Europe and Asia to Africa, 1959–61. Bull World Health Organ 24:197–212PubMedPubMedCentralGoogle Scholar
  36. Ioannou I, Sandalakis V, Kassinis N et al (2011) Tick-borne bacteria in mouflons and their ectoparasites in cyprus. J Wildl Dis 47:300–306CrossRefPubMedGoogle Scholar
  37. Kaiser MN, Hoogstraal H, Watson GE (1974) Ticks (Ixodoidea) on migrating birds in Cyprus, fall 1967 and spring 1968, and epidemiological considerations. Bull Entomol Res 64:97–110CrossRefGoogle Scholar
  38. Kartashov MY, Kononova JV, Tishkova FH, Mikryukova TP, Tupota NL, Petrova ID, Ternovoi VA, Loktev VB (2015) Genetic diversity of ticks in the Tajikistan. Department of Molecular Virology for Flaviviruses and Viral Hepatitis, State Research Center of Virology and Biotechnology ‘Vector’, Koltsovo, NovosibirskGoogle Scholar
  39. Kaur H, Chhilar J, Chhillar S (2016) Mitochondrial 16S rDNA based analysis of some hard ticks belonging to genus Hyalomma Koch, 1844 (Acari: Ixodidae). J Adv Parasitol 3:32–48CrossRefGoogle Scholar
  40. Ketchum H, Teel P, Coates C, Strey O, Longnecker M (2009) Genetic variation in 12S and 16S mitochondrial rDNA genes of four geographically isolated populations of gulf coast ticks (Acari: Ixodidae). J Med Entomol 46:482–489CrossRefPubMedGoogle Scholar
  41. Klompen J, Black W, Keirans J, Oliver J (1996) Evolution of ticks. Annu Rev Entomol 41:141–161CrossRefPubMedGoogle Scholar
  42. Klompen J, Oliver J, Keirans J, Homsher P (1997) A re-evaluation of relationships in the Metastriata (Acari: Parasitiformes: Ixodidae). Syst Parasitol 38:1–24CrossRefGoogle Scholar
  43. Klompen J, Black WC, Keirans JE, Norris DE (2000) Systematics and biogeography of hard ticks, a total evidence approach. Cladistics 16:79–102CrossRefGoogle Scholar
  44. Koc S, Aydın L, Cetin H (2015) Tick species (Acari: Ixodida) in Antalya city, Turkey: species diversity and seasonal activity. Parasitol Res 114:2581–2586CrossRefPubMedGoogle Scholar
  45. Kok J, d’Oliveira C, Jongejan F (1993) Detection of the protozoan parasite Theileria annulata in Hyalomma ticks by the polymerase chain reaction. Exp Appl Acarol 17:839–846CrossRefPubMedGoogle Scholar
  46. Krakowetz CN, Dergousoff SJ, Chilton NB (2010) Genetic variation in the mitochondrial 16S rRNA gene of the american dog tick, Dermacentor variabilis (Acari: Ixodidae). J Vector Ecol 35:163–173.  https://doi.org/10.1111/j.1948-7134.2010.00073.x CrossRefPubMedGoogle Scholar
  47. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  48. Le Riche P, Altan Y, Campbell J, Efstathiou G (1974) Ticks (Ixodoidea) of domestic animals in Cyprus. Bull Entomol Res 64:53–63CrossRefGoogle Scholar
  49. Leo SS, Pybus MJ, Sperling FA (2010) Deep mitochondrial DNA lineage divergences within Alberta populations of Dermacentor albipictus (Acari: Ixodidae) do not indicate distinct species. J Med Entomol 47:565–574CrossRefPubMedGoogle Scholar
  50. Leo S, Davis C, Sperling F (2012) Characterization of 14 microsatellite loci developed for Dermacentor albipictus and cross-species amplification in D. andersoni and D. variabilis (Acari: Ixodidae). Conserv Genet Resour 4:379–382CrossRefGoogle Scholar
  51. Logan TM, Linthicum KJ, Bailey CL, Watts DM, Moulton JR (1989) Experimental transmission of Crimean-Congo hemorrhagic fever virus by Hyalomma truncatum Koch. Am J Trop Med Hyg 40:207–212CrossRefPubMedGoogle Scholar
  52. Lu X, Lin XD, Wang JB et al (2013) Molecular survey of hard ticks in endemic areas of tick-borne diseases in China. Ticks Tick Borne Dis 4:288–296CrossRefPubMedGoogle Scholar
  53. Lv J, Wu S, Zhang Y, Chen Y, Feng C, Yuan X, Jia G, Deng J, Wang C, Wang Q, Mei L, Lin X (2014a) Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida). Parasite Vectors 7(1):93CrossRefGoogle Scholar
  54. Lv J, Wu S, Zhang Y, Zhang T, Feng C, Jia G, Lin X (2014b) Development of a DNA barcoding system for the Ixodida (Acari: Ixodida). Mitochondrial DNA 25(2):142–149CrossRefPubMedGoogle Scholar
  55. Mangold A, Bargues M, Mas-Coma S (1997) 18S rRNA gene sequences and phylogenetic relationships of european hard-tick species (Acari: Ixodidae). Parasitol Res 84:31–37CrossRefGoogle Scholar
  56. Mangold AJ, Bargues MD, Mas-Coma S (1998) Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitol Res 84:478–484.  https://doi.org/10.1007/s004360050433 CrossRefPubMedGoogle Scholar
  57. Montagna M, Chouaia B, Pella F, Mariconti M, Pistone D, Fasola M, Epis S (2012) Screening for bacterial DNA in the hard tick Hyalomma marginatum (Ixodidae) from Socotra Island (Yemen): detection of Francisella-like endosymbiont. J Entomol Acarol Res 44:13CrossRefGoogle Scholar
  58. Moss RH, Edmonds JA, Hibbard KA, Manning MR, Rose SK, Van Vuuren DP, Carter TR, Emori S, Kainuma M, Kram T (2010) The next generation of scenarios for climate change research and assessment. Nature 463:747–756CrossRefPubMedGoogle Scholar
  59. Movila A, Alekseev AN, Dubinina HV, Toderas I (2013) Detection of tick-borne pathogens in ticks from migratory birds in the Baltic region of Russia. Med Vet Entomol 27(1):113–117CrossRefPubMedGoogle Scholar
  60. Murrell A, Campbell N, Barker S (1999) Molecular evolution of the internal transcribed spacer 2 and phylogenetic relationships among species of the tick subfamily Rhipicephalinae. In: The annual scientific meeting of the Australian society for parasitology, the Aust. Society for Parasitology, p 42Google Scholar
  61. Murrell A, Campell NJH, Barker SC (2000) Phylogenetic analyses of the rhipicephaline ticks indicate that the genus Rhipicephalus is paraphyletic. Mol Phylogenet Evol 12(1):83–86CrossRefGoogle Scholar
  62. Nava S, Guglielmone AA, Mangold AJ (2009) An overview of systematics and evolution of ticks. Front Biosci 14:2857–2877CrossRefGoogle Scholar
  63. Nava S, Venzal JM, Labruna MB et al (2010) Hosts, distribution and genetic divergence (16S rDNA) of Amblyomma dubitatum (Acari: Ixodidae). Exp Appl Acarol 51:335–351CrossRefPubMedGoogle Scholar
  64. Norris DE, Klompen J, Keirans JE, Black WC (1996) Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. J Med Entomol 33:78–89CrossRefPubMedGoogle Scholar
  65. Norris DE, Klompen JSH, Black WC (1999) Comparison of the mitochondrial 12S and 16S ribosomal DNA genes in resolving phylogenetic relationships among hard-ticks (Acari: Ixodidae). Ann Entomol Soc Am 92:117–129CrossRefGoogle Scholar
  66. Orkun O (2015) Some ecological and epidemiological data belonging to tick species in Ankara and around. Veterinary Faculty, Ankara University, AnkaraGoogle Scholar
  67. Pegram RG, Hoogstraal H, Wassef HY (1981) Ticks (Acari: Ixodoidea) of Ethiopia. I. Distribution, ecology and host relationships of species infesting livestock. Bull Entomol Res 71:339–359CrossRefGoogle Scholar
  68. Pons J, Barraclough TG, Gomez-Zurita J et al (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609CrossRefPubMedGoogle Scholar
  69. Randolph S (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129:37–65CrossRefGoogle Scholar
  70. Randolph SE, Rogers DJ (2010) The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol 8:361–371CrossRefPubMedGoogle Scholar
  71. Randolph S, Green R, Hoodless A, Peacey M (2002) An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 32:979–989CrossRefPubMedGoogle Scholar
  72. Shyma KP, Kumar S, Sharma AK, Ray DD, Ghosh S (2012) Acaricide resistance status in Indian isolates of Hyalomma anatolicum. Exp Appl Acarol 58(4):471–481CrossRefPubMedGoogle Scholar
  73. Sievers F, Wilm A, Dineen D et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol 7:539CrossRefPubMedPubMedCentralGoogle Scholar
  74. Sonenshine DE, Lane R, Nicholson W (2002) Ticks (ixodida). In: Mullen G, Durden L (eds) Medical and veterinary entomology. Academia, Orlando, pp 517–558CrossRefGoogle Scholar
  75. Šumilo D, Bormane A, Asokliene L, Lucenko I, Vasilenko V, Randolph S (2006) Tick-borne encephalitis in the Baltic States: identifying risk factors in space and time. Int J Med Microbiol 296:76–79CrossRefPubMedGoogle Scholar
  76. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and g + c-content biases. Mol Biol Evol 9:678–687PubMedGoogle Scholar
  77. Tian Z, Liu G, Xie J, Yin H, Luo J, Zhang L, Zhang P, Luo J (2011) Discrimination between Haemaphysalis longicornis and H. qinghaiensis based on the partial 16S rDNA and the second internal transcribed spacer (its-2). Exp Appl Acarol 54:165–172CrossRefPubMedGoogle Scholar
  78. Toma L, Mancini F, Di Luca M, Cecere JG, Bianchi R, Khoury C, Quarchioni E, Manzia F, Rezza G, Ciervo A (2014) Detection of microbial agents in ticks collected from migratory birds in central Italy. Vector Borne Zoonotic Dis 14(3):199–205CrossRefPubMedPubMedCentralGoogle Scholar
  79. Turell MJ (2007) Role of ticks in the transmission of Crimean-Congo hemorrhagic fever virus Crimean-Congo hemorrhagic fever. Springer, Berlin, pp 143–154Google Scholar
  80. Walker AR, Bouattour A, Camicas J et al (2003) Ticks of domestic animals in Africa: a guide to identification of species. Bioscience Reports, EdinburghGoogle Scholar
  81. Wesson DM, McLain DK, Oliver JH, Piesman J, Collins FH (1993) Investigation of the validity of species status of Ixodes dammini (Acari: Ixodidae) using rDNA. PNAS 90:10221–10225CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Division of Ecology, Department of Biology, Faculty of ScienceHacettepe UniversityAnkaraTurkey

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