Forthcoming

Molecular phylogeny of Dermacentor, Haemaphysalis, Hyalomma, and Rhipicephalus hard tick genera

Authors

  • Liu Zhi-Qiang Institute of Veterinary Medicine, Xinjiang Academy of Animal Science
  • She Xiao-Lan
  • Wang Jun-Wei
  • Gao Tian-Qing
  • Guo Hui-Ling
  • Ruan Yong-Lei
  • Kuermanali Nuer
  • Wang Yuan-Zhi
  • Zheng Wen-Xin
  • Zhao Li
  • Wang Bing-Jie

Keywords:

Metastriata, Haemaphysalis chordeilis, Haemaphysalis punctata, synonym, Xinjiang, China

Abstract

Hard ticks (Ixodidae: Metastriata) are ectoparasites of major medical and veterinary importance, but the status and relationships of many lineages remain debated. For this study, we collected 49 tick specimens belonging to 12 species, spanning four genera: Dermacentor, Haemaphysalis, Hyalomma, and Rhipicephalus. Their mitochondrial cox1 and 16S rRNA genes were sequenced and combined with GenBank data to conduct detailed phylogenetic analyses of these four genera. We found strong indications that unidentified Dermacentor sp. specimens may belong to a genetically distinct subspecies of D. nuttalli, or even a different species, with a relatively wide distribution in Xinjiang, China. Dermacentor niveus and Dermacentor marginatus did not exhibit clear genetic separation. Or results support the validity of the genus Alloceraea (comprising a proportion of current Haemaphysalis species). We report first evidence from molecular data that Haemaphysalis chordeilis and Haemaphysalis punctata might be synonymous, and there may exist an unrecognized subspecies or even species within the nominal Haemaphysalis sulcata clade. Two pairs of Hyalomma species were indistinguishable using our molecular datasets: H. turanicum + H. marginatum, and H. anatolicum + H. excavatum. There was no evidence for a subspecies structuring within the Hyalomma asiaticum clade. Multiple nominal species within the Rhipicephalus genus were genetically indistinguishable in our analyses. In conclusion, the taxonomy of metastriate ticks remains deeply problematic, but taxonomic revision is rendered very difficult by the fact that molecular databases are plagued by taxonomic artefacts and insufficient data.

References

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389

Apanaskevich, D. A., Filippova, N. A., & Horak, I. G. (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 Parasitologica, 57(1), 69–78. https://doi.org/10.14411/fp.2010.009

Apanaskevich, D. A., & Horak, I. G. (2010). The genus Hyalomma. XI. Redescription of all parasitic stages of H. (Euhyalomma) asiaticum (Acari: Ixodidae) and notes on its biology. Experimental and Applied Acarology, 52(2), 207–220. https://doi.org/10.1007/s10493-010-9361-0

Bakkes, D. K., Chitimia-Dobler, L., Matloa, D., Oosthuysen, M., Mumcuoglu, K. Y., Mans, B. J., & Matthee, C. A. (2020). Integrative taxonomy and species delimitation of Rhipicephalus turanicus (Acari: Ixodida: Ixodidae). International Journal for Parasitology, 50(8), 577–594. https://doi.org/10.1016/j.ijpara.2020.04.005

Barker, S. C., & Murrell, A. (2004). Systematics and evolution of ticks with a list of valid genus and species names. Parasitology, 129(S1), S15–S36. https://doi.org/10.1017/S0031182004005207

Ben Said, M., Galai, Y., Mhadhbi, M., Jedidi, M., de la Fuente, J., & Darghouth, M. A. (2012). Molecular characterization of Bm86 gene orthologs from Hyalomma excavatum, Hyalomma dromedarii and Hyalomma marginatum marginatum and comparison with a vaccine candidate from Hyalomma scupense. Veterinary Parasitology, 190(1), 230–240. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6141297/. https://doi.org/10.1016/j.vetpar.2012.05.017

Burger, T. D., Shao, R., & Barker, S. C. (2013). Phylogenetic analysis of the mitochondrial genomes and nuclear rRNA genes of ticks reveals a deep phylogenetic structure within the genus Haemaphysalis and further elucidates the polyphyly of the genus Amblyomma with respect to Amblyomma sphenodonti and A. Ticks and Tick-Borne Diseases, 4(4), 265–274. https://doi.org/10.1016/j.ttbdis.2013.02.002

Burger, T. D., Shao, R., Beati, L., Miller, H., & Barker, S. C. (2012). Phylogenetic analysis of ticks (Acari: Ixodida) using mitochondrial genomes and nuclear rRNA genes indicates that the genus Amblyomma is polyphyletic. Molecular Phylogenetics and Evolution, 64(1), 45–55. https://doi.org/10.1016/j.ympev.2012.03.004

Charrier, N. P., Hermouet, A., Hervet, C., Agoulon, A., Barker, S. C., Heylen, D., Toty, C., McCoy, K. D., Plantard, O., & Rispe, C. (2019). A transcriptome-based phylogenetic study of hard ticks (Ixodidae). Scientific Reports, 9(1), Article 1. https://doi.org/10.1038/s41598-019-49641-9

Choubdar, N., Karimian, F., Koosha, M., & Oshaghi, M. A. (2021). An integrated overview of the bacterial flora composition of Hyalomma anatolicum, the main vector of CCHF. PLOS Neglected Tropical Diseases, 15(6), e0009480. https://doi.org/10.1371/journal.pntd.0009480

Cruickshank, R. H. (2002). Molecular markers for the phylogenetics of mites and ticks. Systematic and Applied Acarology, 7(1), 3–14. https://doi.org/10.11158/saa.7.1.1

Dantas-Torres, F., de Sousa-Paula, L. C., & Otranto, D. (2024). The Rhipicephalus sanguineus group: Updated list of species, geographical distribution, and vector competence. Parasites & Vectors, 17(1), 540. https://doi.org/10.1186/s13071-024-06572-3

Egizi, A., & Maestas, L. P. (2022). Where have all the grouse ticks gone? Apparent decline in collections of Haemaphysalis chordeilis Packard. International Journal for Parasitology: Parasites and Wildlife, 19, 323–329. https://doi.org/10.1016/j.ijppaw.2022.11.007

Guglielmone, A. A., & Nava, S. (2014). Names for Ixodidae (Acari: Ixodoidea): Valid, synonyms, incertae sedis, nomina dubia, nomina nuda, lapsus, incorrect and suppressed names-with notes on confusions and misidentifications. Zootaxa, 3767(1), 1–256. https://doi.org/10.11646/zootaxa.3767.1.1

Guglielmone, A. A., Petney, T. N., & Robbins, R. G. (2020). Ixodidae (Acari: Ixodoidea): Descriptions and redescriptions of all known species from 1758 to December 31, 2019. Zootaxa, 4871(1), Article 1. https://doi.org/10.11646/zootaxa.4871.1.1

Guglielmone, A. A., Robbins, R. G., Apanaskevich, D. A., Petney, T. N., Estrada-Peňa, A., Horak, I. G., Shao, R., & Barker, S. C. (2010). The argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: A list of valid species names. Zootaxa, 2528(2528), 1–28. https://doi.org/10.1023/A:1025381712339

Hebert, P. D. N., Ratnasingham, S., & de Waard, J. R. (2003). Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(suppl_1), S96–S99. https://doi.org/10.1098/rsbl.2003.0025

HEKİMOĞLU, O. (2024). An update on the phylogeny and biogeographical history of Rhipicephalus sanguineus complex. Turkish Journal of Zoology, 48(1), 21–35. https://doi.org/10.55730/1300-0179.3157

Hekimoglu, O., & Ozer, A. N. (2017). Distribution and phylogeny of Hyalomma ticks (Acari: Ixodidae) in Turkey. Experimental and Applied Acarology, 73(3), 501–519. https://doi.org/10.1007/s10493-017-0192-0

Jakovlić, I., Zou, H., Ye, T., Zhang, H., Liu, X., Xiang, C.-Y., Wang, G.-T., & Zhang, D. (2023). Mitogenomic evolutionary rates in Bilateria are influenced by parasitic lifestyle and locomotory capacity. Nature Communications, 14(1), Article 1. https://doi.org/10.1038/s41467-023-42095-8

Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., Von Haeseler, A., & Jermiin, L. S. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6), 587–589. https://doi.org/10.1038/nmeth.4285

Karataş, A. (2020). A systematic investigation on the ticks (Acari: Ixodida) of the domestic sheep in Niğde Province, Turkey. Journal of Wildlife and Biodiversity, 31–40. https://doi.org/10.22120/jwb.2020.130348.1162

Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. https://doi.org/10.1093/molbev/mst010

Kelava, S., Apanaskevich, D. A., Shao, R., Gofton, A. W., Mans, B. J., Teo, E. J. M., Norval, G., Barker, D., Nakao, R., & Barker, S. C. (2024). Insights from entire mitochondrial genome sequences into the phylogeny of ticks of the genera Haemaphysalis and Archaeocroton with the elevation of the subgenus Alloceraea Schulze, 1919 back to the status of a genus. Medical and Veterinary Entomology, 38(2), 189–204. https://doi.org/10.1111/mve.12708

Kelava, S., Mans, B. J., Shao, R., Barker, D., Teo, E. J. M., Chatanga, E., Gofton, A. W., Moustafa, M. A. M., Nakao, R., & Barker, S. C. (2023). Seventy-eight entire mitochondrial genomes and nuclear rRNA genes provide insight into the phylogeny of the hard ticks, particularly the Haemaphysalis species, Africaniella transversale and Robertsicus elaphensis. Ticks and Tick-Borne Diseases, 14(2), 102070. https://doi.org/10.1016/j.ttbdis.2022.102070

Kelava, S., Mans, B. J., Shao, R., Moustafa, M. A. M., Matsuno, K., Takano, A., Kawabata, H., Sato, K., Fujita, H., Ze, C., Plantard, O., Hornok, S., Gao, S., Barker, D., Barker, S. C., & Nakao, R. (2021). Phylogenies from mitochondrial genomes of 120 species of ticks: Insights into the evolution of the families of ticks and of the genus Amblyomma. Ticks and Tick-Borne Diseases, 12(1), 101577. https://doi.org/10.1016/j.ttbdis.2020.101577

Kulakova, N. V., Khasnatinov, M. A., Sidorova, E. A., Adel`shin, R. V., & Belikov, S. I. (2014). Molecular identification and phylogeny of Dermacentor nuttalli (Acari: Ixodidae). Parasitology Research, 113(5), 1787–1793. https://www.researchgate.net/publication/260611193_Molecular_identification_and_phylogeny_of_Dermacentor_nuttalli_Acari_Ixodidae. https://doi.org/10.1007/s00436-014-3824-x

Letunic, I., & Bork, P. (2021). Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Research, 49(W1), W293–W296. https://doi.org/10.1093/nar/gkab301

Liu, Z.-Q., Liu, Y.-F., Kuermanali, N., Wang, D.-F., Chen, S.-J., Guo, H.-L., Zhao, L., Wang, J.-W., Han, T., Wang, Y.-Z., Wang, J., Shen, C.-F., Zhang, Z.-Z., & Chen, C.-F. (2018). Sequencing of complete mitochondrial genomes confirms synonymization of Hyalomma asiaticum asiaticum and kozlovi, and advances phylogenetic hypotheses for the Ixodidae. PLOS ONE, 13(5), e0197524. https://doi.org/10.1371/journal.pone.0197524

Lu, X., Zhang, Q., Jiang, D., Liu, Y., Chen, B., Yang, S., Shao, Z., Jiang, H., Wang, J., Fang, Y., Du, C., & Yang, X. (2022). Complete mitogenomes and phylogenetic relationships of Haemaphysalis nepalensis and Haemaphysalis yeni. Frontiers in Veterinary Science, 9, 1007631.

Lv, J., Wu, S., Zhang, Y., Chen, Y., Feng, C., Yuan, X., Jia, G., Deng, J., Wang, C., Wang, Q., Mei, L., & Lin, X. (2014). Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida). Parasites & Vectors, 7(1), 93. https://doi.org/10.1186/1756-3305-7-93

Mangold, A. J., Bargues, M. D., & Mas-Coma, S. (1998). Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae). Parasitology Research, 84(6), 478–484. https://www.researchgate.net/publication/13624999_Mitochondrial_16S_rDNA_sequences_and_phylogenetic_relationships_of_species_of_Rhipicephaus_and_other_tick_genera_among_Metastriata_Acari_Ixodidae. https://doi.org/10.1007/s004360050433

Mans, B. J., de Castro, M. H., Pienaar, R., de Klerk, D., Gaven, P., Genu, S., & Latif, A. A. (2016). Ancestral reconstruction of tick lineages. Ticks and Tick-Borne Diseases, 7(4), 509–535. https://doi.org/10.1016/j.ttbdis.2016.02.002

Minh, B. Q., Nguyen, M. A. T., & von Haeseler, A. (2013). Ultrafast Approximation for Phylogenetic Bootstrap. Molecular Biology and Evolution, 30(5), 1188–1195. https://doi.org/10.1093/molbev/mst024

Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020). IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Molecular Biology and Evolution, 37(5), 1530–1534. https://doi.org/10.1093/molbev/msaa015

Morales, H. E., Pavlova, A., Joseph, L., & Sunnucks, P. (2015). Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Molecular Ecology, 24(11), 2820–2837. https://doi.org/10.1111/mec.13203

Moshaverinia, A., Shayan, P., Nabian, S., & Rahbari, S. (2009). Genetic evidence for conspecificity between Dermacentor marginatus and Dermacentor niveus. Parasitology Research, 105(4), 1125–1132. https://doi.org/10.1007/s00436-009-1532-8

Norris, D. E., Klompen, J. S. H., & Black, W. C. (1999). Comparison of the Mitochondrial 12S and 16S Ribosomal Dna Genes in Resolving Phylogenetic Relationships among Hard Ticks (Acari: Ixodidae). Annals of the Entomological Society of America, 92(1), 117–129. https://doi.org/10.1093/aesa/92.1.117

Okonechnikov, K., Golosova, O., Fursov, M., & the UGENE team. (2012). Unipro UGENE: A unified bioinformatics toolkit. Bioinformatics, 28(8), 1166–1167. https://doi.org/10.1093/bioinformatics/bts091

Orkun, Ö., Sarıkaya, E., Yılmaz, A., Yiğit, M., & Vatansever, Z. (2025). Population genetic structure and demographic history of Dermacentor marginatus Sulzer, 1776 in Anatolia. Scientific Reports, 15(1), 12570. https://doi.org/10.1038/s41598-025-97658-0

Price, M. N., Dehal, P. S., & Arkin, A. P. (2010). FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments. PLOS ONE, 5(3), e9490. https://doi.org/10.1371/journal.pone.0009490

Ratnasingham, S., & Hebert, P. D. N. (2007). bold: The Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes, 7(3), 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x

Sands, A. F., Apanaskevich, D. A., Matthee, S., Horak, I. G., Harrison, A., Karim, S., Mohammad, M. K., Mumcuoglu, K. Y., Rajakaruna, R. S., Santos-Silva, M. M., & Matthee, C. A. (2017). Effects of tectonics and large scale climatic changes on the evolutionary history of Hyalomma ticks. Molecular Phylogenetics and Evolution, 114, 153–165. https://doi.org/10.1016/j.ympev.2017.06.002

Thompson, A. T., Dominguez, K., Cleveland, C. A., Dergousoff, S. J., Doi, K., Falco, R. C., Greay, T., Irwin, P., Lindsay, L. R., Liu, J., Mather, T. N., Oskam, C. L., Rodriguez-Vivas, R. I., Ruder, M. G., Shaw, D., Vigil, S. L., White, S., & Yabsley, M. J. (2020). Molecular Characterization of Haemaphysalis Species and a Molecular Genetic Key for the Identification of Haemaphysalis of North America. Frontiers in Veterinary Science, 7, 141.

Tufts, D. M., & Diuk-Wasser, M. A. (2021). First hemispheric report of invasive tick species Haemaphysalis punctata, first state report of Haemaphysalis longicornis, and range expansion of native tick species in Rhode Island, USA. Parasites & Vectors, 14(1), 394. https://doi.org/10.1186/s13071-021-04887-z

Vatansever, Z. (2017). Haemaphysalis sulcata Canestrini and Fanzago, 1877 (Figs. 91–93). In A. Estrada-Peña, A. D. Mihalca, & T. N. Petney (Eds), Ticks of Europe and North Africa: A Guide to Species Identification (pp. 243–247). Springer International Publishing. https://doi.org/10.1007/978-3-319-63760-0_47

Wang, F., Wang, D., Guo, G., Hu, Y., Wei, J., & Liu, J. (2019). Species delimitation of the Dermacentor ticks based on phylogenetic clustering and niche modeling. PeerJ, 7, e6911. https://doi.org/10.7717/peerj.6911

Wang, J., Chai, Y., Yang, J., Chen, K., Liu, G., Luo, J., Guan, G., Ren, Q., & Yin, H. (2023). Insight into Hyalomma anatolicum biology by comparative genomics analyses. International Journal for Parasitology, In Press. https://doi.org/10.1016/j.ijpara.2023.09.003

Xiang, C., Gao, F., Jakovlić, I., Lei, H., Hu, Y., Zhang, H., Zou, H., Wang, G. T., & Zhang, D. (2023). Using PhyloSuite for molecular phylogeny and tree‐based analyses. iMeta, 2, e87. https://doi.org/10.1002/imt2.87

Zhang, D., Gao, F., Jakovlić, I., Zou, H., Zhang, J., Li, W. X., & Wang, G. T. (2020). PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20(1), 348–355. https://doi.org/10.1111/1755-0998.13096

Zhang, D., Jakovlić, I., Zou, H., Liu, F., Xiang, C.-Y., Gusang, Q., Tso, S., Xue, S., Zhu, W.-J., Li, Z., Wu, J., & Wang, G.-T. (2024). Strong mitonuclear discordance in the phylogeny of Neodermata and evolutionary rates of Polyopisthocotylea. International Journal for Parasitology, 54(5), 213–223. https://doi.org/10.1016/j.ijpara.2024.01.001

Zhang, R. L., & Zhang, B. (2014). Prospects of using DNA barcoding for species identification and evaluation of the accuracy of sequence databases for ticks (Acari: Ixodida). Ticks and Tick-Borne Diseases, 5(3), 352–358. https://doi.org/10.1016/j.ttbdis.2014.01.001

Zhang, X., Miao, W., Xi, C., & GePing, L. (2010). Biological diversity in Kazakhstan and Xinjiang. Arid Land Geography, 33(2), 183–188.

Published

2026-03-09

How to Cite

Zhi-Qiang, L., Xiao-Lan, S., Jun-Wei, W., Tian-Qing, G., Hui-Ling, G., Yong-Lei, R., Nuer, K., Yuan-Zhi, W., Wen-Xin, Z., Li, Z., & Bing-Jie, W. (2026). Molecular phylogeny of Dermacentor, Haemaphysalis, Hyalomma, and Rhipicephalus hard tick genera. Journal of Wildlife and Biodiversity, 9(X). Retrieved from https://wildlife-biodiversity.com/index.php/jwb/article/view/1028

Issue

Vol. 9 No. X (2026): Articles in Press

Section

Original Article

License

Copyright (c) 2022 Journal of Wildlife and Biodiversity

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.