On the Origin of soft ticks (Parasitiformes, Ixodoidea, Argasidae)

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The origin of the common evolutionary branch of soft and hard ticks is dated to the later Permian, approximately coinciding with the Permian extinction, and divergence of the common branch of Ixodoidea into ancestral forms of Argasidae and Ixodidae occurred in the Triassic.

Ancestors of the common branch of Ixodoidea (Ixodidae, Argasidae, Nuttalliellidae) were not bloodsucking arthropods and were closely related to modern representatives of Holothyridae. Bloodsucking and, later, temporary ectoparasitism had developed only after divergence of the main branches (Ixodidae, Argasidae and Nuttalliellidae), independently in each group.

At early stages of the soft tick evolution, bloodsucking was a short-time process, long-time feeding had developed later in larvae and promoted dispersal of ticks. Maintenance of the short-time feeding can be explained by adaptation to dwelling in bird nests or in shelters visited by birds, and later, also in mammal burrows. Displacements of gnathosomе to the ventral side of idiosome hampered combing of a parasite from the host during short-time bloodsucking. Short-time feeding resulted in maintenance and development of coxal glands as the main organ for removal of superfluous liquid during bloodsucking.

Adaptation to shelter habitats (nests, burrows, rock crevices, under dead tree cork, etc.) promoted development of polyphagia and adaptations for long-term starvation.

Full Text

Restricted Access

About the authors

S. A. Leonovich

Зоологический институт РАН

Author for correspondence.
Email: leonssa@mail.ru
Russian Federation, Университетская наб., 1, Санкт-Петербург, 199034

References

  1. Балашов Ю.С. 2009. Паразитизм клещей и насекомых на наземных позвоночныхю СПб, Наука, 357 с. [Balashov Yu.S. 2009. Parazitism kleshchei i nasekomykh na nazemnykh pozvonochnykh. St Petersburg: Nauka, 357 p. (In Russian)].
  2. Григорьева Л.А. 2015. Особенности развития таёжного клеща (Ixodes persulcatus Sch.: Ixodinae: Ixodidae) в условиях природных битопов Ленинградской области. Труды Зоологического института РАН 319 (2): 269–281. [Grigoryeva L.A. 2015. Osobennosti razvitiya taezhnogo kleshcha (Ixodes persulcatus Sch.: Ixodinae: Ixodidae) v usloviyakh prirodnykh biotopov Leiningradskoi oblasti. Trudy Zoologicheskogo instituta RAN 319 (2): 269–281. (In Russian)]. https://doi.org/10.31610/trudyzin/2015.319.2.269
  3. Леонович С.А. 2019. О типах паразитизма иксодовых клещей (Ixodidae). Паразитология 53 (5): 416–420. [Leonovich S.A. 2019. Types of parasitism of hard ticks (Ixodidae). Parazitologiya 53 (5): 416–420. (In Russian)]. https://doi.org/10.1134/S0031184719050053.
  4. Леонович С.А. 2023. О происхождении иксодовых клещей (Parasitiformes, Ixodidae). Паразитология 57 (2): 91–107. [Leonovich S.A. 2003. On the origin of ixodid ticks (Parasitiformes, Ixodidae). Parazitologiya 57 (2): 91–107. (In Russian)]. doi: 10.31857/S0031184723020011; EDN: AZSEGK
  5. Наумов Р.Л. 2006. Продолжительность жизни клеща Ixodes ricinus (Acari: Ixodidae) в центральной России. Паразитология 40 (4): 384–395. [Naumov R.L. 2006. The longevity of the tick Ixodes ricinus (Acari: Ixodidae) in central Russia. Parazitologiya 40 (4): 384–395. (In Russian)].
  6. Поспелова-Штром М.В. 1953. Клещи-орнитодорины и их эпидемиологическое значение. М., 1953 [Pospelova-Shtrom M.V. 1953. Kleshchi-ornotodorony i ikh epidemiologicheskoe znachernie, Nauka, Moscow, 1953 (In Russian)].
  7. Филиппова Н.А. 1966. Аргасовые клещи (Argasidae). Фауна СССР. Паукообразные. Т. IV, вып. 3. Ленинград, Наука, 251 с. [Filippova N.A. 1966. Argasovye kleshchi (Argasidae). Fauna SSSR. Paukoobraznye. V. 4, № 3, Leningrad, Nauka, 251 pp. (In Russian)].
  8. Audy R.F., Radovsky F.J., Vercammen-Grandjean P.H. 1972. Neosomy: radical intrastadial metamorphosis associated with arthropod symbioses. Journal of Medical Entomology 9 (6): 487–494. https://doi.org/10.1093/jmedent/9.6.487
  9. Barker S.C., Murrel A., 2004. Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129 Suppl.: 15–36. doi: 10.1017/s0031182004005207
  10. Barker S.C., Murrel A. 2008. Systematics and evolution of ticks with a list of valid genus and species names. In: Bowman A., Nutall P. (Eds). Ticks: biology, disease and control. Cambridge University Press. 325 pp. DOI: https://doi.org/10.1017/CBO9780511551802.002
  11. Barker S., Walker A.R. 2014. Ticks of Australia. The species that infest domestic animals and humans. Zootaxa 3816 (1): 1–144. doi: 10.11646/zootaxa.3816.1.1
  12. Beati L., Klompen H. 2019. Phylogeography of Ticks (Acari: Ixodida). Annual Review of Entomology 64: 379–97. https://doi.org/10.1146/annurev-ento-020117-043027
  13. Burger T.D., Shao R., Labruna M.B., Barker S.C. 2014. Molecular phylogeny of soft ticks (Ixodida: Argasidae) inferred from mitochondrial genome and nuclear rRNA sequences. Ticks and Tick–Borne Diseases 5 (2): 195–207. doi: 10.1016/j.ttbdis.2013.10.009
  14. Chitimia-Dobler L., Mans B.J., Handschuh S., Dunlop J.A. 2022. A remarkable assemblage of ticks from mid-Cretaceous Burmese amber. Parasitology 149: 820–830. https://doi.org/10.1017/S0031182022000269
  15. Dusbabek F., Leonovich S.A. 1988. Circadian basis of assembly pheromone response in Argas (Persicargas) persicus. Experimental and Applied Acarology 4: 319–334.
  16. El Shoura S.M., Hoogstraal H., Roshdy M.A. 1984. Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): female internal morphology. Journal of Parasitology 70: 114–120.
  17. Estrada-Peña A., Mangold A.J., Nava S., José M., Venzal J.M., Labruna M., Guglielmone A.A. 2010. A review of the systematics of the tick family Argasidae (Ixodida). Acarologia 50 (3): 317–333. doi: 10.1051/acarologia/20101975
  18. Galun R., Sternberg S., Mango C. 1978. Effects of host spectra on feeding behaviour and reproduction of soft ticks (Acari: Argasidae). Bulletin of Entomological Research 68 (1): 153 – 157. DOI: https://doi.org/10.1017/S0007485300007239
  19. Guglielmone A.A., Robbins R.G., Apanaskevich D.A., Petney T.N., Estrada-Peña 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: 1–28.
  20. Hoogstraal H. 1985. Argasid and nuttallelid ticks as parasites and vectors. Advances in parasitology 24: 135–238.
  21. Horak I.G., Camicao J.-L., Keirans J.E. 2002. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida): A world list of valid tick names. Experimental and Applied Acarology 28 (1–4): 27–54. doi: 10.1023/a:1025381712339
  22. Hornok S., Murányi D., Kontschán J., Vuong Tan Tu. 2019. Description of the male and the larva of Ixodes collaris Hornok, 2016 with drawings of all stages. Parasites & Vectors 12: 144. https://doi.org/10.1186/s13071-019-3365-3
  23. Kaufman W.R., Flynn P.C., Reynolds S.E. 2010. Cuticular plasticization in the tick, Amblyomma hebraeum (Acari: Ixodidae): possible roles of monoamines and cuticular pH. Journal of Experimental Biology 213 (16): 2820–2831. https://doi.org/10.1242/jeb.044412
  24. Klompen H., 2010. Holothyrids and ticks: new insights from larval morphology and DNA sequencing, with the description of a new species of Diplothyrus (Parasitiformes: Neothyridae). Acarologia 50(2): 269–285. doi: 10.1051/acarologia/20101970
  25. Klompen J.S.H., Oliver Jr J.H. 1993. Systematic relationships in the soft ticks (Acari: Ixodida: Argasidae). Systematic Entomology 18 (4): 313–331. https://doi.org/10.1111/j.1365-3113.1993.tb00669.x
  26. Klompen H., Grimaldi D., 2001. First Mesozoic record of a parasitiform mite: a larval argasid tick in Ccretaceous amber (Acari: Ixodida: Argasidae). Annals of Entomological Society of America 94 (1): 10–15. https://doi.org/10.1603/0013-8746(2001)094[0010:FMROAP]2.0.CO;2
  27. Latif A.A., Putterill J.F., de Klerk D.G., Pienaar R., Mans B.J. 2012. Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): first description of the male, immature stages and re-description of the female. PLoS ONE 7(7): e41651. https://doi.org/10.1371/journal.pone.0041651
  28. Lehtinen P. 1991. Revision of the old world Holothyridae (Arachnida : Anactinotrichida : Holothyrina). Invertebrate Taxonomy 9 (4): 767–826. https://doi.org/10.1071/IT9950767
  29. Mans B.J., Andersen J.F., Francischetti I.M.B., Valenzuela J.G., Schwan T.G., Pham V.M., Garfield M.K., Hammer C.H., Ribeiro J.M.C. 2008. Comparative sialomics between hard and soft ticks: Implications for the evolution of blood-feeding behavior. Insect Biochemistry and Molecular Biology 38 (1): 42–58. https://doi.org/10.1016/j.ibmb.2007.09.003t
  30. Mans B.J., de Klerk D., Pienaar R., Latif A.A. 2011. Nuttalliella namaqua: a living fossil and closest relative to the ancestral tick lineage: implications for the evolution of blood-feeding in ticks. PLoS ONE 6(8): e23675. https://doi.org/10.1371/journal.pone.0023675
  31. Mans B.J., de Castro M.H., Pienaar R., de Klerk D., Gaven P., Genu S., et al. 2016. Ancestral reconstruction of tick lineages. Ticks Tick Borne Dis. 7: 509–535. doi: 10.1016/j.ttbdis.2016.02.002
  32. Mans B.J., Featherston J.cC, Kvas M., Pillay R.-A., de Klerk D.G., Pienaar R., de Castro M.H., Schwan T.G., Lopez J.E., Teel P., Pérez de León A.A., Sonenshine D.E., Egekwu N.I., Bakkes D.K., Heyne H., Kanduma E.G., Nyangiwe N., Bouattour A., Latif A.A. 2019. Argasid and ixodid systematics: Implications for soft tick evolution and systematics, with a new argasid species list. Ticks and Tick-borne Diseases 10 (1): 219–240. https://doi.org/10.1016/j.ttbdis.2018.09.010
  33. Mans B.J., Kelava S., Pienaar R., Featherston J., de Castro M.H., Quetglas J., Reeves W.K., Durden L.A., Miller M.M., Laverty T.M., Shao R., Takano A., Kawabata H., Moustafa M.A.M., Nakao R., Matsuno K., Greay T.L., Evasco K.L., Barker D., Barker S.C. 2021. Nuclear (18S-28S rRNA) and mitochondrial genome markers of Carios (Carios) vespertilionis (Argasidae) support Carios Latreille, 1796 as a lineage embedded in the Ornithodorinae: re-classification of the Carios sensu Klompen and Oliver (1993) clade into its respective subgenera. Ticks and Tick–Borne Diseases 12 (4): 101688. doi: 10.1016/j.ttbdis.2021.101688
  34. Manzano-Román R., Díaz-Martín V., de la Fuente J., Pérez-Sánchez R. 2012. Soft ticks as pathogen vectors: distribution, surveillance and control. In: Parasitology (Ed. by M.M. Shah). Open Acess. doi: 10.5772/32521
  35. Peñalver E., Arillo A., Delclòs X., Peris D., Grimaldi D.A., Anderson S.R., Nascimbene P.C., Pérez-de la Fuente R. 2017. Ticks parasitized feathered dinosaurs as revealed by Cretaceous amber assemblages. Nature Communications 8: 1924. doi: 10.1038/s41467-017-01550-z
  36. Poinar G. 1995. First fossil soft tick, Ornithodoros antiquus n. sp. (Acari: Argasidae) in Dominican amber with evidence of their mammalian host. Cellular and Molecular Life Sciences 51 (4): 384–387. doi: 10.1007/BF01928900
  37. Pugh P.J.A. 1997. Spiracle structure in ticks (Ixodida: Anactinotrichida: Arachnida): Resume, taxonomic and functional significance. Biological Reviews of Cambridge Philosophical Society 72: 549–564. doi: 10.1017/s0006323197005094
  38. Ribeiro J.M.R., Labruna M.B., Mans B.J., Maruyama S.R., Francischetti I.M.B., Barizon G.C., de Miranda Santos I.K.F. 2012. The sialotranscriptome of Antricola delacruzi female ticks is compatible with non-hematophagous behavior and an alternative source of food. I nsect Biochemistry and Molecular Biology 42 (3): 332–342. https://doi.org/10.1016/j.ibmb.2012.01.003
  39. Rothschild M. 1992. Neosomy in fleas, and the sessile life-style. Journal of Zoology 226 (4): 613–629. https://doi.org/10.1111/j.1469-7998.1992.tb07504.x
  40. Sándor A.D., Mihalca A.D., Domşa C., Péter Á., Hornok S. 2021. Argasid ticks of palearctic bats: distribution, host selection, and zoonotic importance. Frontiers in Veterinary Science 8: 684737. doi: 10.3389/fvets.2021.684737
  41. Sonenshine D.E., Clifford G.M., Kohls G.M. 1962. The identification of larvae of the genus Argas (Acarina: Argasidae). Acarologia 4 (2): 193–214.
  42. Shepherd J.G. 2021. Record longevity and reproduction of an African tick, Argas brumpti (Ixodida: Argasidae). Journal of Medical Entomology 59 (2): 777–778. doi: 10.1093/jme/tjab205
  43. Vial l. 2009. Biological and ecological characteristics of soft ticks (Ixodida: Argasidae) and their impact for predicting tick and associated disease distribution. Parasite 16: 191–202. http://dx.doi.org/10.1051/parasite/2009163191
  44. Woodring J.P. 1973. Comparative morphology, function and homologies of the coxal glands of Oribatid mites (Arachnida, Acari). Journal of Morphology 139: 407–429. doi: 10.1002/jmor.1051390404

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure 1. The main morphological characters of ticks: (A–B) soft ticks, with an example of the genus Ornithodoros (А – dorsal view, B – ventral view) and (С–D) hard ticks, with an example of a female of the genus Hyalomma (C – dorsal view, В – ventral view). From Barker, Walker, 2014. Designations: (gn) gnathosoma; (scu) scutum; (cl) claw; (soi) soft idiosoma; (pu) pulvillus.

Download (411KB)
Indexing metadata
3. Figure 2. External view of soft (A–B) and hard (C–D) tick larvae. Left – dorsal view; right – ventral view. A – larva of Argas brevipes (from Sonenshine et al., 1962). В – larva of Ixodes collaris (from Hornok et al., 2019). Designations as in Fig. 1.

Download (361KB)
Indexing metadata

Copyright (c) 2024 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies