{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T02:29:15Z","timestamp":1760149755307,"version":"build-2065373602"},"reference-count":50,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,9,7]],"date-time":"2023-09-07T00:00:00Z","timestamp":1694044800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Science and Higher Education of Russia","award":["0837-2019-0007"],"award-info":[{"award-number":["0837-2019-0007"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Widely distributed Ixodes ricinus and Ixodes persulcatus ticks transmit many pathogens of both medical and veterinary significance. The ranges of these tick species overlap and form large sympatric areas in the East European Plain and Baltic countries. It has previously been shown that crossing I. ricinus and I. persulcatus is possible, resulting in the appearance of sterile hybrids. In the present study, we analyzed the features of this hybrid\u2019s life cycle under laboratory conditions. For this purpose, virgin females of I. ricinus and I. persulcatus ticks were obtained in the laboratory, and hybrid generations of ticks were bred from the reciprocal crossings of these two tick species. According to our data, mating the females of I. ricinus and I. persulcatus with the males of another species leads to a decrease in the engorgement success of the females, a decrease in the number of hatched larvae, and the appearance of a hybrid generation in which both females and males are sterile. Under laboratory conditions at a constant room temperature and under natural daylight, the morphogenetic diapause of the engorged I. persulcatus larvae began in September. For I. persulcatus nymphs, it occurred earlier than for I. ricinus, in October and November, respectively. The hybrids generally repeated the features of the life cycle of the mother species.<\/jats:p>","DOI":"10.3390\/microorganisms11092252","type":"journal-article","created":{"date-parts":[[2023,9,7]],"date-time":"2023-09-07T09:56:36Z","timestamp":1694080596000},"page":"2252","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Development Features of Ixodes ricinus \u00d7 I. persulcatus Hybrids under Laboratory Conditions"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9040-0774","authenticated-orcid":false,"given":"Oxana A.","family":"Belova","sequence":"first","affiliation":[{"name":"Laboratory of Biology of Arboviruses, FSASI \u201cChumakov FSC R&D IBP RAS\u201d (Institute of Poliomyelitis), 108819 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexandra E.","family":"Polienko","sequence":"additional","affiliation":[{"name":"Laboratory of Biology of Arboviruses, FSASI \u201cChumakov FSC R&D IBP RAS\u201d (Institute of Poliomyelitis), 108819 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anastasia D.","family":"Averianova","sequence":"additional","affiliation":[{"name":"Laboratory of Biology of Arboviruses, FSASI \u201cChumakov FSC R&D IBP RAS\u201d (Institute of Poliomyelitis), 108819 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Galina G.","family":"Karganova","sequence":"additional","affiliation":[{"name":"Laboratory of Biology of Arboviruses, FSASI \u201cChumakov FSC R&D IBP RAS\u201d (Institute of Poliomyelitis), 108819 Moscow, Russia"},{"name":"Institute for Translational Medicine and Biotechnology, Sechenov University, 119991 Moscow, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,9,7]]},"reference":[{"key":"ref_1","first-page":"396","article-title":"Ixodid Ticks of the Subfamily Ixodinae","volume":"4","author":"Filippova","year":"1977","journal-title":"Fauna SSSR New Ser."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"102114","DOI":"10.1016\/j.ttbdis.2022.102114","article-title":"The Biology of Ixodes ricinus with Emphasis on Its Ecology","volume":"14","author":"Kahl","year":"2023","journal-title":"Ticks Tick. Borne. Dis."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"100508","DOI":"10.1016\/j.onehlt.2023.100508","article-title":"Geographical Distribution of Ixodes persulcatus and Associated Pathogens: Analysis of Integrated Data from a China Field Survey and Global Published Data","volume":"16","author":"Wang","year":"2023","journal-title":"One Health"},{"key":"ref_4","first-page":"223","article-title":"The Sympatry of Closely Related Species of Ixodid Ticks and Its Possible Role in the Parasitic Systems of Natural Foci of Transmissible Diseases","volume":"33","author":"Filippova","year":"1999","journal-title":"Parazitologiia"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"556","DOI":"10.1186\/s13071-018-3131-y","article-title":"Tick-Borne Pathogens in Finland: Comparison of Ixodes ricinus and I. persulcatus in Sympatric and Parapatric Areas","volume":"11","author":"Laaksonen","year":"2018","journal-title":"Parasites Vectors"},{"key":"ref_6","first-page":"36","article-title":"Vectors of Tick-Borne Diseases and Epidemiological Situation in Latvia in 1993\u20132002","volume":"293","author":"Bormane","year":"2004","journal-title":"Int. J. Med. Microbiol. Suppl."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Katargina, O., Russakova, S., Geller, J., Kondrusik, M., Zajkowska, J., Zygutiene, M., Bormane, A., Trofimova, J., and Golovljova, I. (2013). Detection and Characterization of Tick-Borne Encephalitis Virus in Baltic Countries and Eastern Poland. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061374"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"630","DOI":"10.1016\/j.ttbdis.2015.05.007","article-title":"New Localities of Dermacentor reticulatus Ticks in the Baltic Countries","volume":"6","author":"Paulauskas","year":"2015","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1080\/13921657.2002.10512509","article-title":"Forms of Sympatry and Possible Ways of Microevolution of Closely Related Species of The Group Ixodes ricinus\u2014persulcatus (Ixodidae)","volume":"12","author":"Filippova","year":"2002","journal-title":"Acta Zool. Litu."},{"key":"ref_10","unstructured":"Balashov, Y.S. (1998). Ixodid Ticks\u2014Parasites and Vectors of Diseases, Nauka. (In Russian)."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"992","DOI":"10.1016\/j.ttbdis.2016.05.006","article-title":"Diapause in Ticks of the Medically Important Ixodes kicinus Species Complex","volume":"7","author":"Gray","year":"2016","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1023\/A:1006070416135","article-title":"The Ecology of Ticks Transmitting Lyme Borreliosis","volume":"22","author":"Gray","year":"1998","journal-title":"Exp. Appl. Acarol."},{"key":"ref_13","unstructured":"Sonenshine, D.E., and Roe, R.M. (2013). Biology of Ticks, Oxford University Press. [2nd ed.]."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Kahl, O., Levin, M., and Beard, C.B. (2023). An Annotated Reprint of Yu. S. Balashov\u2019s 1972 Book Bloodsucking Ticks (Ixodoidea)\u2014Vectors of Diseases of Man and Animals, Entomological Society of America.","DOI":"10.4182\/UZSO8298"},{"key":"ref_15","unstructured":"Filippova, N.A. (1985). Taiga Tick Ixodes persulcatus Schulze (Acarina, Ixodidae): Morphology, Systematics, Ecology, Medical Importance, Nauka. (In Russian)."},{"key":"ref_16","unstructured":"Obenchain, F.D., and Galun, R. (1982). Physiology of Ticks, Pergamon Press."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-3305-6-1","article-title":"Driving Forces for Changes in Geographical Distribution of Ixodes ricinus Ticks in Europe","volume":"6","author":"Medlock","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_18","first-page":"3","article-title":"Diapause and Quiescence as Two Main Kinds of Dormancy and Their Significance in Life Cycles of Mites and Ticks (Chelicerata: Arachnida: Acari). Part 2. Parasitiformes","volume":"17","author":"Belozerov","year":"2009","journal-title":"Acarina"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1134\/S0013873816050109","article-title":"Geographic Variability of Morphogenetic Diapause in Larvae and Nymphs of the Taiga Tick Ixodes persulcatus (Acarina, Ixodidae)","volume":"96","author":"Korotkov","year":"2016","journal-title":"Entomol. Rev."},{"key":"ref_20","first-page":"500","article-title":"Reproductive Isolation and Interspecific Hybridization in Ixodid Ticks of the Ixodes ricinus\u2014I. persulcatus Group (Acarina, Ixodidae)","volume":"78","author":"Balashov","year":"1998","journal-title":"Entomol. Rev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1298882","DOI":"10.1080\/22423982.2017.1298882","article-title":"Impact of Air Temperature Variation on the Ixodid Ticks Habitat and Tick-Borne Encephalitis Incidence in the Russian Arctic: The Case of the Komi Republic","volume":"76","author":"Tokarevich","year":"2017","journal-title":"Int. J. Circumpolar Health"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/1756-3305-5-8","article-title":"Changes in the Geographical Distribution and Abundance of the Tick Ixodes ricinus during the Past 30 Years in Sweden","volume":"5","author":"Jaenson","year":"2012","journal-title":"Parasites Vectors"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.ttbdis.2012.07.004","article-title":"Distribution of Ixodes ricinus and I. persulcatus Ticks in Southern Karelia (Russia)","volume":"4","author":"Bugmyrin","year":"2013","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/j.ttbdis.2017.10.002","article-title":"Distribution of Ixodes ricinus Ticks and Prevalence of Tick-Borne Encephalitis Virus among Questing Ticks in the Arctic Circle Region of Northern Norway","volume":"9","author":"Soleng","year":"2018","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"101388","DOI":"10.1016\/j.ttbdis.2020.101388","article-title":"The Distribution Limit of the Common Tick, Ixodes ricinus, and Some Associated Pathogens in North-Western Europe","volume":"11","author":"Hvidsten","year":"2020","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/emi.2017.17","article-title":"Crowdsourcing-Based Nationwide Tick Collection Reveals the Distribution of Ixodes ricinus and I. persulcatus and Associated Pathogens in Finland","volume":"6","author":"Laaksonen","year":"2017","journal-title":"Emerg. Microbes Infect."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e9538","DOI":"10.1002\/ece3.9538","article-title":"Does Environmental Adaptation or Dispersal History Explain the Geographical Distribution of Ixodes ricinus and Ixodes persulcatus Ticks in Finland?","volume":"12","author":"Kulha","year":"2022","journal-title":"Ecol. Evol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"370","DOI":"10.1111\/zph.12696","article-title":"Geographical Distribution and Prevalence of Tick-Borne Encephalitis Virus in Questing Ixodes ricinus Ticks and Phylogeographic Structure of the Ixodes ricinus Vector in Norway","volume":"67","author":"Vikse","year":"2020","journal-title":"Zoonoses Public Health"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Voyiatzaki, C., Papailia, S.I., Venetikou, M.S., Pouris, J., Tsoumani, M.E., and Papageorgiou, E.G. (2022). Climate Changes Exacerbate the Spread of Ixodes ricinus and the Occurrence of Lyme Borreliosis and Tick-Borne Encephalitis in Europe\u2014How Climate Models Are Used as a Risk Assessment Approach for Tick-Borne Diseases. Int. J. Environ. Res. Public Health, 19.","DOI":"10.3390\/ijerph19116516"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1186\/1756-3305-6-202","article-title":"Borrelia burgdorferi sensu lato Prevalence in Tick Populations in Estonia","volume":"6","author":"Geller","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1007\/BF00051934","article-title":"Differences in Borrelia Infections in Adult Ixodes persulcatus and Ixodes ricinus Ticks (Acari: Ixodidae) in Populations of North-Western Russia","volume":"19","author":"Kovalevskii","year":"1995","journal-title":"Exp. Appl. Acarol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1128\/JCM.39.6.2237-2242.2001","article-title":"Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes Ticks in the Baltic Regions of Russia","volume":"39","author":"Alekseev","year":"2001","journal-title":"J. Clin. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.ttbdis.2012.08.003","article-title":"Association between Anaplasma phagocytophilum Seroprevalence in Dogs and Distribution of Ixodes ricinus and Ixodes persulcatus Ticks in Latvia","volume":"4","author":"Berzina","year":"2013","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"216","DOI":"10.1016\/j.ttbdis.2015.10.013","article-title":"Siberian Subtype Tick-Borne Encephalitis Virus in Ixodes ricinus in a Newly Emerged Focus, Finland","volume":"7","author":"Tonteri","year":"2016","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/j.ttbdis.2015.09.005","article-title":"Natural Hybridization between Ixodes ricinus and Ixodes persulcatus Ticks Evidenced by Molecular Genetics Methods","volume":"7","author":"Kovalev","year":"2016","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/j.ttbdis.2014.11.001","article-title":"Morphological Differentiation of Ixodes persulcatus and I. ricinus Hybrid Larvae in Experiment and under Natural Conditions","volume":"6","author":"Bugmyrin","year":"2015","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1007\/s10493-016-0036-3","article-title":"Morphological Features of Ixodes persulcatus and I. ricinus Hybrids: Nymphs and Adults","volume":"69","author":"Bugmyrin","year":"2016","journal-title":"Exp. Appl. Acarol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Litov, A.G., Belova, O.A., Bugmyrin, S.V., Kholodilov, I.S., Romanova, L.I., and Karganova, G.G. (2022). Differentiation of Laboratory-Obtained Ixodes ricinus \u00d7 Ixodes persulcatus Hybrid Ticks: Selection of Suitable Genes. Microorganisms, 10.","DOI":"10.3390\/microorganisms10071306"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1111\/mve.12096","article-title":"Divergent Host Preferences of Above- and below-Ground Culex pipiens Mosquitoes and Their Hybrid Offspring","volume":"29","author":"Fritz","year":"2015","journal-title":"Med. Vet. Entomol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1104484","DOI":"10.3389\/fcimb.2023.1104484","article-title":"Hybrids of Ixodes ricinus and Ixodes persulcatus Ticks Effectively Acquire and Transmit Tick-Borne Encephalitis Virus","volume":"13","author":"Belova","year":"2023","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.ttbdis.2012.05.005","article-title":"Different Tick-Borne Encephalitis Virus (TBEV) Prevalences in Unfed versus Partially Engorged Ixodid Ticks\u2014Evidence of Virus Replication and Changes in Tick Behavior","volume":"3","author":"Belova","year":"2012","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1016\/j.ttbdis.2017.07.008","article-title":"Properties of the Tick-Borne Encephalitis Virus Population during Persistent Infection of Ixodid Ticks and Tick Cell Lines","volume":"8","author":"Belova","year":"2017","journal-title":"Ticks Tick-Borne Dis."},{"key":"ref_43","first-page":"161","article-title":"Bloodsucking Ticks (Ixodoidea)-Vectors of Disease in Man and Animals (English Translation)","volume":"8","author":"Balashov","year":"1972","journal-title":"Misc. Publ. Entomol. Soc. Am."},{"key":"ref_44","first-page":"409","article-title":"Sexual Dimorphism of the Larvae and Nymphs of the Taiga Tick\u2014Ixodes persulcatus","volume":"20","author":"Voltsit","year":"1986","journal-title":"Parazitologiia"},{"key":"ref_45","first-page":"153","article-title":"Influence of Microclimatic Factors on the Development and Virus Infection Rate of Ticks Ixodes ricinus (L.) under Experimental Conditions","volume":"30","author":"Daniel","year":"1983","journal-title":"Folia Parasitol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1134\/S0013873822020117","article-title":"Thermal Constants of Development of Ixodes persulcatus and Ixodes ricinus Ticks, Which Determine the Duration of Their Life Cycle and Their Distribution","volume":"102","author":"Sirotkin","year":"2022","journal-title":"Entomol. Rev."},{"key":"ref_47","first-page":"85","article-title":"Establishment of a Laboratory Colony of Taiga Tick Ixodes persulcatus for Tick-Borne Pathogen Transmission Studies","volume":"55","author":"Konnai","year":"2008","journal-title":"Jpn. J. Vet. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1017\/S003118200002357X","article-title":"Ixodes ricinus in Relation to Its Physical Environment: The Influence of Climate on Development","volume":"26","author":"Macleod","year":"1934","journal-title":"Parasitology"},{"key":"ref_49","first-page":"357","article-title":"Development of Some Tick Species under Standard Laboratory Conditions","volume":"18","year":"1971","journal-title":"Folia Parasitol."},{"key":"ref_50","first-page":"346","article-title":"On the Question of Seasonal Appearances in the Life of the Ticks Ixodes ricinus L. and I. persulcatus P. Sch","volume":"4","author":"Babenko","year":"1956","journal-title":"Med. Parazitol. Parazit. Bolezn."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/9\/2252\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:46:54Z","timestamp":1760129214000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/11\/9\/2252"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,7]]},"references-count":50,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["microorganisms11092252"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms11092252","relation":{},"ISSN":["2076-2607"],"issn-type":[{"type":"electronic","value":"2076-2607"}],"subject":[],"published":{"date-parts":[[2023,9,7]]}}}