Abstract
Ticks are important ectoparasites responsible for the transmission of several pathogens with significant medical, veterinary, and economic impacts. Climate and social changes have generated substantial changes in ticks’ distribution, abundance, and activity patterns, including ticks belonging to the Hyalomma marginatum species. Knowledge on the genetic structure and dynamics of H. marginatum populations might contribute to a better understanding of their current and future evolution under the effects of anthropogenic factors and eco-climatic changes. In the present study, we investigated the genetic structure and phylogenetic distribution of H. marginatum across three bioclimatic regions in Tunisia using two mitochondrial markers (16S and 12S rRNA). The molecular investigations were based on 47 adult H. marginatum ticks collected from humid, upper semi-arid, and sub-humid regions of Tunisia. Our results revealed a genetic diversity of 0.278% and 0.809% using the 16S and 12S markers, respectively. The low genetic diversity that we observed raises the hypothesis of a bottleneck event occasioned by a reduction in the size of the tick population under the effects of environmental factors and/or human activities. This hypothesis is supported by the population’s demographic history analysis, which revealed a clear deviation from neutrality and supports the occurrence of a bottleneck event followed by a demographic expansion. The fact that most 16S and 12S variability was present in the ticks from the humid bioclimatic zone may suggest that those ticks represent the ancestral population. Overall, the analysis has shown that the phylogenetic clusters do not correspond to the bioclimatic zones.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The nucleotide sequence data reported in this study are available in the GenBank under the NCBI accession numbers OQ263353, OQ263356–OQ263362, and OQ269607–OQ269616 for the 12S and 16S sequences, respectively.
References
Apanaskevich DA, Horak IG (2009) 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
Araya-Anchetta A, Busch JD, Scoles GA, Wagner DM (2015) Thirty years of tick population genetics: a comprehensive review. Infect Genet Evol 29:164–179. https://doi.org/10.1016/j.meegid.2014.11.008
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
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 87:32–48. https://doi.org/10.1645/0022-3395(2001)087[0032:aotsra]2.0.co;2
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 12:514–525. https://doi.org/10.1089/vbz.2011.0859
Belkahia H, Ben Said M, Alberti A et al (2015) First molecular survey and novel genetic variants’ identification of Anaplasma marginale, A. centrale and A. bovis in cattle from Tunisia. Infect Genet Evol 34:361–371. https://doi.org/10.1016/j.meegid.2015.06.017
Ben Said M, Galai Y, Mhadhbi M et al (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. Vet Parasitol 190:230–240. https://doi.org/10.1016/J.VETPAR.2012.05.017
Birungi J, Munstermann LE (2002) Genetic structure of Aedes albopictus (Diptera: Culicidae) populations based on mitochondrial ND5 sequences: evidence for an independent invasion into Brazil and United States. Ann Entomol Soc Am 95:130–132. https://doi.org/10.1603/0013-8746(2002)095[0125:gsoaad]2.0.co;2
Bouaicha F, Eisenbarth A, Elati K, Schulz A, Ben Smida B, Bouajila M, Sassi L, Rekik M, Groschup MH, Khamassi Khbou M (2021) Epidemiological investigation of Crimean-Congo haemorrhagic fever virus infection among the one-humped camels (Camelus dromedarius) in southern Tunisia. Ticks Tick Borne Dis 12. https://doi.org/10.1016/J.TTBDIS.2020.101601
Bouattour, M A Darghouth, A Daouad (1999) Distribution and ecology of ticks (Acari: Ixodidae) infesting livestock in Tunisia: an overview of eighth years field collections. Parassitologia 41(Suppl 1):5–10. https://pubmed.ncbi.nlm.nih.gov/11071534/.
Chard Gendris R (2019) Arachnida 257–377. https://doi.org/10.1016/B978-0-12-813890-00004-3
Chhillar S, Singh J, Kaur H (2014) Investigations on some hard ticks (Acari: Ixodidae) infesting domestic buffalo and cattle from Haryana, India. J Entomol Zool Stud 2:99–104
Choubdar N, Karimian F, Koosha M et al (2021) Hyalomma spp. ticks and associated Anaplasma spp. and Ehrlichia spp. on the Iran-Pakistan border. Parasit Vectors 14:1–8. https://doi.org/10.1186/s13071-021-04956-3
De La Fuente J, Estrada-Pena A, Venzal JM et al (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946. https://doi.org/10.2741/3200
Domşa C, Sándor AD, Mihalca AD (2016) Climate change and species distribution: possible scenarios for thermophilic ticks in Romania. Geospat Health 11:151–156. https://doi.org/10.4081/GH.2016.421
Estrada-Peña A, Sánchez N, Estrada-Sánchez A (2012) An assessment of the distribution and spread of the tick hyalomma marginatum in the western Palearctic under different climate scenarios. Vector-Borne Zoonotic Dis 12:758–768. https://doi.org/10.1089/vbz.2011.0771
Estrada-Peña A, De La Fuente J, Latapia T, Ortega C (2015) The impact of climate trends on a tick affecting public health: a retrospective modeling approach for Hyalomma marginatum (Ixodidae). Plos One 10:e0125760 https://doi.org/10.1371/JOURNAL.PONE.0125760
Estrada-Peña A, D’Amico G, Palomar AM et al (2017) A comparative test of ixodid tick identification by a network of European researchers. Ticks Tick Borne Dis 8:540–546. https://doi.org/10.1016/j.ttbdis.2017.03.001
Fernández-Ruiz N, Estrada-Peña A (2021) Towards new horizons: climate trends in Europe increase the environmental suitability for permanent populations of Hyalomma marginatum (Ixodidae). Pathogens 10:1–13. https://doi.org/10.3390/PATHOGENS10020095
Forster P, Torroni A, Renfrew C, Röhl A (2001) Phylogenetic star contraction applied to Asian and Papuan mtDNA evolution. Mol Biol Evol 18:1864–1881
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925. https://doi.org/10.1093/genetics/147.2.915
Giorgi F (2006) Climate change hot-spots. Geophys Res Lett 33:8707. Available from https://doi.org/10.1029/2006GL025734
Guglielmone AA, Apanaskevich DA, Estrada-Peña A et al (2014) The hard ticks of the world: (Acari: Ixodida: Ixodidae). Springer, Dordrecht, pp 1–738
Harpending HC (2013) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Published by: Wayne State University Press. Hum Biol 66:591–600. http://www.jstor.org/stable/41465371
Hekimoglu O (2018) Distribution and phylogeny of Hyalomma ticks (Acari: Ixodidae) in Turkey distribution and phylogeny of Hyalomma ticks (Acari: Ixodidae) in Turkey. Exp Appl Acarol 73:501–519. https://doi.org/10.1007/s10493-017-0192-0
Hornok S, Horváth G (2012) First report of adult Hyalomma marginatum rufipes (vector of Crimean-Congo haemorrhagic fever virus) on cattle under a continental climate in Hungary. Parasit Vectors 5:2–5. https://doi.org/10.1186/1756-3305-5-170
Hosseini A, Dalimi A, Abdigoudarzi M (2011) Morphometric study on male specimens of Hyalomma anatolicum (Acari: Ixodidae) in West of Iran. Iranian J Arthropod-Borne Dis 5(2):23–31
Hosseini-Chegeni A (2021) An illustrated guide to identification of ticks (Acari: Ixodidae & Argasidae) the species that infest domestic animals in Iran. GlobeEdit (56):9786200625571
Hosseini-Chegeni A, Hosseini R, Tavakoli M, Telmadarraiy Z, Abdigoudarzi M (2013) The Iranian Hyalomma (Acari: Ixodidae) with a key to the identification of male species. PJA 2:503–529
Hosseini-Chegeni A, Hosseini R, Abdigoudarzi M, Telmadarraiy Z, Tavakoli M (2015) An additional records of Hyalomma marginatum rufipes Koch, 1844 (Acari: Ixodidae) in southwestern and southern Iran with a molecular evidence. Iran J Anim Biosystematics 11(1):79–89
Hosseini Chegeni A, Hosseini R, Telmadarraiy Z, Mohammad A (2019a). The Iranian Hyalomma (Acari: Ixodidae) with molecular evidences to understand taxonomic status of species complexes. Persian J Acarol 8:291–308. http://www.biotaxa.org/pja
Hosseini-Chegeni A, Tavakoli M, Telmadarraiy Z (2019b) The updated list of ticks (Acari: Ixodidae & Argasidae) occurring in Iran with a key to the identification of species. Sys Appl Acarol 24–11. https://doi.org/10.11158/saa.24.11.8
Jaouad M (2004) Dynamique des cheptels bovins en tunisie et contraintes alimentaires et fourragères. Cah Options Méditeranniennes 424:421–424
Joshi J, Salar RK, Banerjee P et al (2013) Genetic variation and phylogenetic relationships of Indian buffaloes of Uttar Pradesh. Asian-Australasian J Anim Sci 26:1229–1236. https://doi.org/10.5713/ajas.2012.12669
Kumar B, Manjunathachar HV, Ghosh S (2020) A review on Hyalomma species infestations on human and animals and progress on management strategies. Heliyon 6:e05675. https://doi.org/10.1016/J.HELIYON.2020.E05675
Latif AA, Walker AR (2004) An introduction to the biology and control of ticks in Africa. ICTTD-2 Project, 1–29. References - Scientific Research Publishing. Available from: https://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=1828959
Leblebicioglu H, Ozaras R, Erciyas-Yavuz K (2015) Emergence of Crimean-Congo hemorrhagic fever. Trans R Soc Trop Med Hyg 109:676–678. https://doi.org/10.1093/trstmh/trv083
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Livanova NN, Tikunov AY, Kurilshikov AM et al (2015) Genetic diversity of Ixodes pavlovskyi and I. persulcatus (Acari: Ixodidae) from the sympatric zone in the south of Western Siberia and Kazakhstan. Exp Appl Acarol 67:441–456. https://doi.org/10.1007/S10493-015-9947-7
Lv J, Wu S, Zhang Y et al (2014) Development of a DNA barcoding system for the Ixodida (Acari: Ixodida). Mitochondrial DNA 25:142–149. https://doi.org/10.3109/19401736.2013.792052
Márquez FJ, Caruz A (2021) Phylogeography of Hyalomma (Euhyalomma) lusitanicum (Acarina, Parasitiformes, Ixodidae) in Andalusia based on mitochondrial cytochrome oxidase I gene. Exp Appl Acarol 85:49–61
Naim DM, Kamal NZM, Mahboob S (2020) Population structure and genetic diversity of Aedes aegypti and Aedes albopictus in Penang as revealed by mitochondrial DNA cytochrome oxidase I. Saudi J Biol Sci 27:953–967. https://doi.org/10.1016/j.sjbs.2020.01.021
Navajas M, Fenton B (2000) The application of molecular markers in the study of diversity in acarology: a review. Exp Appl Acarol 24:751–774
Nei M, Maruyama T, Chakraborty R (2012) The bottleneck effect and genetic variability in populations. Society for the study of evolution stable. Evolution (N Y) 29:1–10. http://www.jstor.org/stable/2407137
Norris DE, Klompen JSH, Keirans JE, Black WC IV (1996) Population genetics of Ixodes scapularis (Acari: Ixodidae) based on mitochondrial 16S and 12S genes. J Med Entomol 33:78–89. https://doi.org/10.1093/jmedent/33.1.78
Ogden NH, Lindsay LR, Hanincová K et al (2008) Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol 74:1780–1790. https://doi.org/10.1128/AEM.01982-07
Orkun Ö (2018) Molecular characterization based on 16S rDNA phylogeny of some ixodid ticks in Turkey. Turkiye Parazitolojii Derg 42:121–129. https://doi.org/10.5152/tpd.2018.5882
Páez-Triana L, Muñoz M, Herrera G et al (2021) Genetic diversity and population structure of Rhipicephalus sanguineus sensu lato across different regions of Colombia. Parasit Vectors 14:1–11. https://doi.org/10.1186/s13071-021-04898-w
Parola P, Raoult D (2001) Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis 32:897–928. https://doi.org/10.1086/319347
Polzin T, Daneschmand SV (2003) On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett 31:12–20
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034
Randolph SE, Rogers DJ (2000) Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. Proc R Soc B Biol Sci 267:1741–1744. https://doi.org/10.1098/rspb.2000.1204
Rivera-Páez FA, Labruna MB, Martins TF et al (2018) Contributions to the knowledge of hard ticks (Acari: Ixodidae) in Colombia. Ticks Tick Borne Dis 9:57–66. https://doi.org/10.1016/J.TTBDIS.2017.10.008
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569. https://doi.org/10.1093/OXFORDJOURNALS.MOLBEV.A040727
Roth A, Akad F, Zonstein I et al (2019) Molecular characterization of six Hyalomma species using mitochondrial markers. Ticks Tick Borne Dis 10:911–917. https://doi.org/10.1016/j.ttbdis.2019.04.015
Sands AF, Apanaskevich DA, Matthee S et al (2017a) Effects of tectonics and large scale climatic changes on the evolutionary history of Hyalomma ticks. Mol Phylogenet Evol 114:153–165. https://doi.org/10.1016/j.ympev.2017.06.002
Sands AF, Apanaskevich DA, Matthee S et al (2017b) The effect of host vicariance and parasite life history on the dispersal of the multi-host ectoparasite, Hyalomma truncatum. J Biogeogr 44:1124–1136. https://doi.org/10.1111/jbi.12948
Selmi R, Ben Said M, Ben Yahia H et al (2020) Molecular epidemiology and phylogeny of spotted fever group Rickettsia in camels (Camelus dromedarius) and their infesting ticks from Tunisia. Transbound Emerg Dis 67:733–744. https://doi.org/10.1111/TBED.13392
Shao R, Barker SC (2007) Mitochondrial genomes of parasitic arthropods: implications for studies of population genetics and evolution. Parasitology 134:153–167. https://doi.org/10.1017/S0031182006001429
Stachurski F, Moutailler S, Boissier, Vayssier-Taussat M, Lancelot R, Allienne J-F, Devilliers E, Maestrini O, Marco S (2016) Etude des tiques et maladies transmises en milieu insulaire méditerranéen; l’ exemple du cheptel bovin corse Ticks and tick-borne pathogens on a Mediterranean island environment: the Corsican cattle. pp 35–338
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595. https://doi.org/10.1093/GENETICS/123.3.585
Telahigue K, Hajji T, El Cafsi M, Saavedra C (2018) Genetic structure and demographic history of the endemic Mediterranean scallop Pecten jacobaeus inferred from mitochondrial 16s DNA sequence analysis. Anim Biodivers Conserv 41:61–73. https://doi.org/10.32800/abc.2018.41.0061
Vial L, Stachurski F, Leblond A et al (2016) Strong evidence for the presence of the tick Hyalomma marginatum Koch, 1844 in southern continental France. Ticks Tick Borne Dis 7:1162–1167. https://doi.org/10.1016/j.ttbdis.2016.08.002
Weir W, Ben-Miled L, Karagenç T et al (2007) Genetic exchange and sub-structuring in Theileria annulata populations. Mol Biochem Parasitol 154:170–180. https://doi.org/10.1016/J.MOLBIOPARA.2007.04.015
Žitko T, Kovaćić A, Desdevises Y, Puizina J (2011) Genetic variation in east-Adriatic populations of the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae), inferred from NADH5 and COI sequence variability. Eur J Entomol 108:501–508. https://doi.org/10.14411/eje.2011.065
Acknowledgements
The authors acknowledge the technical assistance of Mr. Mokhtar Dhibi, Mr. Limam Sassi, and Mr. Taoufik Lahmar. The authors also thank the farmers who took part in this study and all the veterinarians for their invaluable assistance.
Funding
This study was financially supported by the project of the CGIAR Research Program on Livestock (CRP Livestock), the Tuniso-Algerian bilateral cooperation project “Comparative analysis of the epidemiology of tropical theileriosis and of Theileria annulata infected cell lines in Tunisia and Algeria”, the Tunisian-Turkish bilateral cooperation “Comparative analysis of the genetic and putative antigenic diversity of Theileria annulata genes encoding immunogenic antigens” and the “Laboratory of Epidemiology of Enzootic Infections in Herbivores in Tunisia: Application to Control” (LR16AGR01) funded by the Ministry of Higher Education and Scientific Research, Tunisia. This study is also carried out as part of the MOBIDOC student allowance program, which is run by the ANPR and funded by the Ministry of Higher Education and Scientific Research through the PromEssE project (Agence Nationale de Promotion de la Recherche Scientifique).
Author information
Authors and Affiliations
Contributions
Conceptualization: Soufiene Chaari, Mourad Rekik, Tarek Hajji, Mohamed Aziz Darghouth.
Formal analysis and investigation: Hayet Benyedem, Isaiah Obara, Moez Mhadhbi, Khawla Elati, Essia Sebai, Rihab Romdhane, Tarek Hajji
Funding acquisition: Soufiene Chaari, Mourad Rekik.
Software: Hayet Benyedem, Tarek Hajji, Issaiah Obara
Supervision: Tarek Hajji, Mohamed Aziz Darghouth
Validation: Moez Mhadhbi, Soufiene Chaari, Mourad Rekik,Tarek Hajji, Mohamed Aziz Darghouth
Visualization: Soufiene Chaari, Mourad Rekik, Mohamed Aziz Darghouth
Writing – original draft: Hayet Benyedem
Writing – review and editing: All authors have reviewed the manuscript.
Corresponding authors
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
All authors have agreed to the content and authorship of the manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Handling Editor: Una Ryan
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Benyedem, H., Hajji, T., Romdhane, R. et al. Genetic diversity of Hyalomma marginatum in Tunisia is not influenced by the bio-climate. Parasitol Res 122, 3013–3025 (2023). https://doi.org/10.1007/s00436-023-07990-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-023-07990-5