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Rhipicephalus annulatus, R. australis or R. microplus? Discordance between morphological and genetic data among three cattle tick species

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Abstract

The taxonomy of ticks of the subgenus Boophilus has been extensively debated and is often complicated by the high intraspecific variation of morphological features between species. Notably, the cattle tick Rhipicephalus microplus is a species complex consisting of Rhipicephalus annulatus, Rhipicephalus australis and the three mitochondrial clades (A-C) of R. microplus. To gain insight into the taxonomic status of this species complex, we performed morphological and molecular analyses on these cattle ticks across four states in peninsular Malaysia. We morphologically identified 60 males and 104 females of R. microplus, 298 males and 374 females of R. australis, and one R. annulatus male in our field collection, of which the latter two species have never been recorded in Malaysia. However, all three morphologically identified species were molecularly assigned as R. microplus clade A based on the barcoding cytochrome oxidase subunit I (COI) analysis. The discrepancy between morphological and genetic data highlights an urgent need for further exploration and in-depth research into the taxonomic status of these sympatric tick species.

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References

  • Aeschlimann A, Morel PC (1965) Boophilus geigyi n. sp. (Acarina: Ixodoidea), a new tick from cattle of West Africa. Acta Trop 22:162–168

    CAS  PubMed  Google Scholar 

  • Ali A, Parizi LF, Ferreira BR, da Silva Vaz Junior I (2016) A revision of two distinct species of Rhipicephalus: R. microplus and R. australis. Ciência Rural 46:1240–1248

    Article  CAS  Google Scholar 

  • Anastos G (1950) The scutate, or Ixodidae, of Indonesia. Entomol Am 30:1–144

    Google Scholar 

  • Arthur DR (1960) Ticks, a monograph of the Ixodoidea. Part V—on the genera Dermacentor, Anocentor, Cosmiomma, Boophilus and Margaropus. Cambridge University Press, London

    Google Scholar 

  • Bakkes DK, Ropiquet A, Chitimia-Dobler L, Matloa DE, Apanaskevich DA, Horak IG, Mans BJ, Matthee CA (2021) Adaptive radiation and speciation in Rhipicephalus ticks: a medley of novel hosts nested predator-prey food webs off-host periods and dispersal along temperature variation gradients. Mol Phylogenet Evol 162:162107178

    Article  Google Scholar 

  • Barker SC, Walker AR (2014) Ticks of Australia: the species that infest domestic animals and humans. Zootaxa 3816(1):1–144

    Article  Google Scholar 

  • Berry CM (2017) Resolution of the taxonomic status of Rhipicephalus (Boophilus) microplus. Dissertation, University of Glasgow

  • Burger TD, Shao R, Barker SC (2014) Phylogenetic analysis of mitochondrial genome sequences indicates that the cattle tick, Rhipicephalus (Boophilus) microplus, contains a cryptic species. Mol Phylogenet Evol 76:241–253

    Article  PubMed  Google Scholar 

  • Davey RB, Osburn RL, Castillo C (1983) Longevity and mating behavior in males and parthenogenesis in females in hybridized Boophilus ticks (Acari: Ixodidae). J Med Entomol 20:614–617

    Article  CAS  PubMed  Google Scholar 

  • Doeve W (1923) De teek op Celebes. Nederland Indisch Bl Diergeneesk 34:17–23

    Google Scholar 

  • Estrada-Peña A, Venzal JM, Nava S, Mangold A, Guglielmone AA, Labruna MB, de la Fuente J (2012) Reinstatement of Rhipicephalus (Boophilus) australis Fuller, the Australian cattle tick (Acari: Ixodidae) with redescription of the adult and larval stages. J Med Entomol 49:794–802

    Article  PubMed  Google Scholar 

  • Fuller C (1899) Notes on the Queensland cattle tick and its relationship to the red water tick and the blue tick of Cape Colony (South Africa). Qld Agric J 4:389–394

    Google Scholar 

  • Graham OH, Price MA, Trevino JL (1972) Cross-mating experiments with Boophilus annulatus and B. microplus (Acarina: Ixodidae). J Med Entomol 9:531–537

    Article  CAS  PubMed  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG (2014) The hard ticks of the world (Acari: Ixodida: Ixodidae). Springer, New York

    Book  Google Scholar 

  • Guzmán PEE, Cuétara CF, Cano Argüelles AL, Castillo AF, Martínez YG, Fernández RR, Afonso YF, Soto YB, Alfaro YG, Méndez L, García AD, Estrada MP, Rodríguez-Mallon A (2021) Characterization of two Cuban colonies of Rhipicephalus microplus ticks. Vet Parasitol Reg Stud Rep 25:100591

    Google Scholar 

  • Heyne H (1987) Differentiation of Boophilus decoloratus and Boophilus microplus. J S Afr Vet Assoc 57:251–252

    Google Scholar 

  • Hoogstraal H (1956) African Ixodoidea 1. Ticks of the Sudan (with special reference to Equatoria Province and with preliminary reviews of Boophilus, Margaropus and Hyalomma). Department of the Navy, Bureau of Medicine and Surgery, Washington DC

    Google Scholar 

  • Hoogstraal H, Kaiser MN (1960) Boophilus kohlsi n. sp. (Acarina: Ixodidae) from sheep and goats in Jordan. J Parasitol 46:441–448

    Article  CAS  PubMed  Google Scholar 

  • Kaewmongkol S, Kaewmongkol G, Inthong N, Lakkitjaroen N (2015) Variation among Bm86 sequences in ticks collected from cattle across Thailand. Exp Appl Acarol 66:1–10

    Article  Google Scholar 

  • Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166

    Article  CAS  PubMed  Google Scholar 

  • Kohls GM (1957) Malaysian parasites. 18. Ticks (Ixodoidea) of Borneo and Malaya. Stud Institut Med Res 28:65–94

    Google Scholar 

  • Koningsberger JC (1900) Onderzoekingen betreffende de teken (Ixodidae) van Nederlandsch-Indië. Teysmannia 11:56–64

    Google Scholar 

  • Kovalev SY, Mikhaylishcheva MS, Mukhacheva TA (2015) Natural hybridization of the ticks Ixodes persulcatus and Ixodes pavlovskyi in their sympatric populations in Western Siberia. Infect Genet Evol 32:388–395

    Article  PubMed  Google Scholar 

  • Kovalev SY, Golovljova IV, Mukhacheva TA (2016) Natural hybridization between Ixodes ricinus and Ixodes persulcatus ticks evidenced by molecular genetics methods. Ticks Tick Borne Dis 7:113–118

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krantz GW, Walter DE (2009) A manual of acarology. Texas Tech University Press, Texas

    Google Scholar 

  • Krijgsman BJ, Ponto SAS (1931) Die Verbreitung der Zecken in Niederländisch-Ostindien. Z Parasitenkd 4:140–146

    Article  Google Scholar 

  • Krijgsman BJ, Ponto SAS (1932) De teken van den Oost-Indischen Archipel. Veeartsenijk Meded 79:1–62

    Google Scholar 

  • Lancaster WE (1939) Report of the Veterinary Department of the Federated Malay States. Fed Malay States 49–52

  • Lempereur L, Geysen D, Madder M (2010) Development and validation of a PCR–RFLP test to identify African Rhipicephalus (Boophilus) ticks. Acta Trop 114:55–58

    Article  CAS  PubMed  Google Scholar 

  • Londt JGH, Arthur DR (1975) The structure and parasitic life cycle of Boophilus microplus (Canestrini, 1888) in South Africa (Acarina: Ixodidae). J Entomol Soc South Afr 38:321–340

    Google Scholar 

  • Low VL, Tay ST, Kho KL, Koh FX, Tan TK, Lim YAL, Ong BL, Chandrawathani P, Yusoff NR, Mohd SA (2015) Molecular characterisation of the tick Rhipicephalus microplus in Malaysia: new insights into the cryptic diversity and distinct genetic assemblages throughout the world. Parasites Vectors 8:1–10

    Article  CAS  Google Scholar 

  • Ma M, Chen Z, Liu A, Ren Q, Liu J, Liu Z, Li Y, Yin H, Guan G, Luo J (2016) Biological parameters of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) fed on rabbits, sheep, and cattle. Korean J Parasitol 54:301–305

    Article  PubMed  PubMed Central  Google Scholar 

  • Minning W (1934) Beiträge zur Systematik und Morphologie der Zeckengattung Boophilus Curtice. Zeitschrift Parasitenk 7:1–43

    Article  Google Scholar 

  • Minning W (1935) Zur Kenntnis des Genus Boophilus Curtice I. Zeitschrift Parasitenk 7:719–721

    Article  Google Scholar 

  • Minning W (1936) Zur Kenntnis des Genus Boophilus Curtice II. Zeitschrift Parasitenk 8:365–370

    Article  Google Scholar 

  • Murrell A, Barker SC (2003) Synonymy of Boophilus Curtice, 1891 with Rhipicephalus Koch, 1844 (Acari: Ixodidae). Syst Parasitol 56:169–172

    Article  PubMed  Google Scholar 

  • Nava S, Venzal JM, González-Acuña D, Martins TF, Guglielmone AA (2017) Ticks of the southern cone of America. Diagnosis, distribution, and hosts with taxonomy, ecology and sanitary importance. Academic Press, Cambridge

    Google Scholar 

  • Neumann LG (1897) Revision de la famille des Ixodides. Mem Soc Zool Fr 10:324–420

    Google Scholar 

  • Neumann LG (1901) Revision de la famille des Ixodides. Mem Soc Zool Fr 14:249–372

    Google Scholar 

  • Nieschulz O (1924) Haemaphysalis bispinosa Neum., nieuw voor de fauna van Nederl-Indie. Tijdschr Diergeneesk 51:195

    Google Scholar 

  • Puillandre N, Brouillet S, Achaz G (2021) ASAP: assemble species by automatic partitioning. Mol Ecol Resour 21:609–620

    Article  PubMed  Google Scholar 

  • Roy BC, Estrada-Peña A, Krücken J, Rehman A, Nijhof AM (2018) Morphological and phylogenetic analyses of Rhipicephalus microplus ticks from Bangladesh, Pakistan and Myanmar. Ticks Tick Borne Dis 9:1069–1079

    Article  PubMed  Google Scholar 

  • Salmon DE, Stiles CW (1901) The cattle ticks (Ixodoidea) of the United States. Annual report of the United States. Department of Agriculture, Bureau of Animal Industry, Washington, pp 380–491

    Google Scholar 

  • Sharif M (1928) A revision of the Indian Ixodidae with special reference to the collection in the Indian Museum. Records Indian Mus 30:217–344

    Google Scholar 

  • Spickett AM, Malan JR (1978) Genetic incompatibility between Boophilus decoloratus (Koch, 1844) and Boophilus microplus (Canestrini, 1888) and hybrid sterility of Australian and South African Boophilus microplus (Acarina: Ixodidae). Onderstepoort J Vet Res 45:149–153

    CAS  PubMed  Google Scholar 

  • Stiles CW, Hassell A (1901) Notes on Parasites, 56: Boophilus australis present in Cuba, Porto Rico, Venezuela, and India. Bureau of Animal Industry, United States Department of Agriculture, Washington

    Google Scholar 

  • Thompson GD, Osburn RL, Davey RB, Drummond RO, Price MA (1981) Hybrid sterility in cattle ticks (Acari: Ixodidae). Experientia 37:127–128

    Article  Google Scholar 

  • Uilenberg G (1962) Boophilus (Uroboophilus) fallax Minning, 1934 synonyme de Boophilus microplus (Canestrini, 1887) (Ixodidae). Rev Elev Med Vet Pays Trop 15:387–398

    Article  Google Scholar 

  • Walker AR, Bouattour A, Camicas JL (2003) Ticks of domestic animals in Africa: a guide to identification of species. The University of Edinburgh, Edinburgh

    Google Scholar 

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Acknowledgements

The authors would like to explicitly express their gratitude to Dr. Sangeetha A/P Sarvananthan from Pusat Ternakan Haiwan (PTH) Ulu Lepar, Pn. Aznida binti Che Ali from Ladang 16, Universiti Putra Malaysia (UPM), Pn. Suriaty binti Ramli from Institut Biodiversiti Veterinar Kebangsaan (IBVK), Pn. Sabariah binti Basir and Dr. Mohd Asraf bin Asmat from Institut Veterinar Malaysia (IVM), En. Taufik Mohd Noor and En. Muhammad Lutfi Zakaria for giving their permissions to visit the farm sites. Sincere thanks to IMMB for the laboratory facilities provided in this study. This study was supported by the Higher Institution Centre of Excellence (HICoE) program (MO002-2019) and Bernhard Nocht Institute for Tropical Medicine from Hamburg, Germany.

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Authors and Affiliations

  1. Department of Medical Microbiology and Parasitology, Faculty of Medicine, Universiti Teknologi MARA Sungai Buloh Campus, Sungai Buloh, Malaysia

    A. R. Kazim, J. Houssaini & C. C. Heo

  2. Higher Institution of Centre of Excellence (HICoE), Tropical Infectious Diseases Research and Education Centre (TIDREC), Universiti Malaya, Kuala Lumpur, Malaysia

    V. L. Low

  3. Bernhard Nocht Institute for Tropical Medicine, Hamburg, Germany

    D. Tappe

  4. Institute of Pathology, Laboratory and Forensic Medicine (I-PPerForM), Universiti Teknologi MARA Sungai Buloh Campus, Sungai Buloh, Malaysia

    J. Houssaini & C. C. Heo

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  1. A. R. Kazim
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Correspondence to C. C. Heo.

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Kazim, A.R., Low, V.L., Tappe, D. et al. Rhipicephalus annulatus, R. australis or R. microplus? Discordance between morphological and genetic data among three cattle tick species. Exp Appl Acarol 87, 119–131 (2022). https://doi.org/10.1007/s10493-022-00726-7

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