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Haemaphysalis cretacea a nymph of a new species of hard tick in Burmese amber

Published online by Cambridge University Press:  12 April 2018

Lidia Chitimia-Dobler ,
Timo Pfeffer  and
Jason A Dunlop
Lidia Chitimia-Dobler
Affiliation:
Bundeswehr Institute of Microbiology, Neuherbergstrasse 11, D-80937 Munich, Germany German Center of Infection Research (DZIF) Partner Munich
Timo Pfeffer
Affiliation:
Keyence Deutschland GmbH, Siemensstrasse 1, 63263 Neu-Isenburg, Germany
Jason A Dunlop*
Affiliation:
Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstrasse 43, D-10115 Berlin, Germany
*
Author for correspondence: Jason A Dunlop, E-mail: jason.dunlop@mfn-berlin.de
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Abstract

The first fossil potentially assignable to the extant hard tick genus Haemaphysalis CL Koch (1844) (Ixodida: Ixodidae) is described from the Late Cretaceous (ca. 99 Ma) Burmese amber of Myanmar. Haemaphysalis (Alloceraea) cretacea sp. nov. is the oldest and only fossil representative of this genus; living members of which predominantly feed on mammals. Their typical hosts are known since at least the Jurassic and the discovery of a mid-Cretaceous parasite, which might have fed on mammals raises again the question of to what extent ticks are coupled to their (modern) host groups. An inferred Triassic split of Argasidae (soft ticks) into the bird-preferring Argasinae and mammal-preferring Ornithodorinae dates to about the time when dinosaurs (later including birds) and mammaliaforms as potential hosts were emerging. Ixodidae may have split into Prostriata and Metastriata shortly after the end-Permian mass extinction, an event which fundamentally altered the terrestrial vertebrate fauna. Prostriata (the genus Ixodes) prefer birds and mammals today, and some may have used groups like cynodonts in the Triassic. Basal metastriate ticks (e.g. Amblyomma) prefer reptiles, but derived metastriates (including Haemaphysalis) again prefer mammals. Here, we may be looking at a younger (Cretaceous?) shift associated with more recent mammalian radiations.

Keywords

CretaceousfossilHaemaphysalishostsIxodidaMetastriataMyanmar
Type
Research Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1440 - 1451
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Copyright © Cambridge University Press 2018 

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References

Abadala, F and Ribeiro, AM (2010) Distribution and diversity patterns of Triassic cynodonts (Therapsida, Cynodontia) in Gondwana. Palaeogeography, Palaeoclimatology and Palaeoecology 286, 202–217.Google Scholar
Aspanaskevich, DA, et al. (2013) First description of the immature stages and redescription of the adults of Cosmiomma hippopotamensis (Acari: Ixodidae) with notes on its bionomics. Journal of Medical Entomology 50, 709–722.Google Scholar
Barker, SC and Murrell, A (2002) Phylogeny, evolution and historical zoogeography of ticks: a review of recent progress. Experimental and Applied Acarology 28, 55–68.Google Scholar
Barker, SC and Murrell, A (2004) Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 129, S15–S36.Google Scholar
Barker, SC, Walker, AR and Campelo, D (2014) A list of the 70 species of Australian ticks; diagnostic guides to and species accounts of Ixodes holocyclus (paralysis tick), Ixodes cornuatus (southern paralysis tick) and Rhipicephalus australis (Australian cattle tick); and consideration of the place of Australia in the evolution of ticks with comments on four controversial ideas. International Journal of Parasitology 44, 941–953.Google Scholar
Beati, L, Keirans, JE and Durden, LA (2008) Bothriocroton oudemansi (Neumann, 1910) n. comb. (Acari: Ixodida: Ixodidae), an ectoparasite of western long-beaked echidna in Papua New Guinea: redescription of the male and first description of the female and nymph. Systematic Parasitology 69, 185–200.Google Scholar
Bedford, GAH (1931) Nuttalliella namaqua, a new genus and species of tick. Parasitology 23, 230–232.Google Scholar
Brocklehurst, N, et al. (2012) The completeness of the fossil record of Mesozoic birds: implications for early avian evolution. PLoS ONE 7(6), e39056.Google Scholar
Burger, TD, Shao, R and Barker, SC (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 Amblyomma elaphense. Ticks and Tick Borne Diseases 4, 265–274.Google Scholar
Burger, TD, et al. (2014) Molecular phylogeny of soft ticks (Ixodida: Argasidae) inferred from mitochondrial genome and nuclear rRNA sequences. Ticks and Tick Borne Diseases 5, 195–207.Google Scholar
Camicas, JL and Morel, PC (1977) Positions systématique et classification des tiques (Acarida: Ixodida). Acarologia 18, 410–420.Google Scholar
Camicas, JL, et al. (1998) Les tiques du monde. Nomenclature, stades décrits, hôtes, répartition (Acarida, Ixodida). Paris: Orstom, 233 pp.Google Scholar
Cerdeño, E (1998) Diversity and evolutionary trends of the family Rhinocerotidae (Perissodactyla). Palaeogeography, Palaeoclimatology and Paleoecology 141, 13–34.Google Scholar
Chitimia-Dobler, L, et al. (2017) Amblyomma birmitum a new species of hard tick in Burmese amber. Parasitology 144, 1411–1448.Google Scholar
Clack, JA (2012) Gaining Ground: The Origin and Evolution of Tetrapods, 2nd edn. Bloomington, Indiana: Indiana University Press.Google Scholar
Clifford, CM, Anastos, G and Elbl, A (1961) The larval ixodid ticks of the Eastern United States (Acarina: Ixodidae). Miscellaneous Publications of the Entomological Society of America 2, 213–237.Google Scholar
Daeschler, EB, Shubin, NH and Jenkins, FA Jr. (2006) A Devonian tetrapod-like fish and the evolution of the tetrapod body plan. Nature 440, 757–763.Google Scholar
de la Fuente, J (2003) The fossil record and the origin of ticks (Acari: Parasitiformes: Ixodida). Experimental and Applied Acarology 29, 331–344.Google Scholar
Dobson, SJ and Barker, SC (1999) Phylogeny of the hard ticks (Ixodidae) inferred from 18S rRNA indicates that the genus Aponomma is paraphyletic. Molecular Phylogenetics and Evolution 11, 288–295.Google Scholar
dos Reis, M, Donoghue, PCJ and Yang, Z (2014) Neither phylogenomic nor palaeontological data support a Palaeogene origin of placental mammals. Biology Letters 10, 20131003.Google Scholar
Dunlop, JA, et al. (2016) Microtomography of the Baltic amber tick Ixodes succineus reveals affinities with the modern Asian disease vector Ixodes ovatus. BMC Evolutionary Biology 16, 203.Google Scholar
El Shoura, SM (1990) Nuttalliella namaqua (Acarina: Ixodoidea: Nuttalliellidae) redescription of the female morphology in relation to the families Argasidae and Ixodidae. Acarologia 31, 349–355.Google Scholar
Emel'yanovat, ND and Hoogstraal, H, (1973) Haemaphysalis verticalis Itagaki, Noda, and Yamaguchi: rediscovery in China, adult and immature identity, rodent hosts, distribution, and medical relationships (Ixodoidea: Ixodidae). Journal of Parasitology 59, 724–733.Google Scholar
Estrada-Peña, A, et al. (2010) A review of the systematics of the tick family Argasidae (Ixodida). Acarologia 50, 317–333.Google Scholar
Evans, SE (1998) Crown group lizards from the Middle Jurassic of Britain. Palaeontographica A 250, 123–154.Google Scholar
Feider, Z (1965) Fauna of the Peoples Republic of Romania. Suprafamily Ixodoidea. Ticks. Ed. Acad. Rep. Pop. Romane, Bucharest, 405 pp. [In Romanian].Google Scholar
Filippova, NA (1997) Ixodid Ticks of Subfamily Amblyomminae. Fauna of Russia and Neighbouring Countries. Arachnoidea. Vol. 4(5). Nauka, St. Petersburg, 244 pp. [In Russian].Google Scholar
Filippova, NA and Bardzimashvily, EA (1992) Anomalohimalaya cricetuli (Ixodoidea: Ixodidae) in the mountains of Middle Asia and differential diagnostics of female and nymph. Parazitologiia 26, 403–408. [Article in Russian].Google Scholar
Filippova, NA and Panova, IV (1978) Anomalohimalaya lotozkyi sp. n., a new species of ixodid ticks from the Peter the First Range (Ixodoidea, Ixodidae). Parazitologiia 12, 391–399. [Article in Russian].Google Scholar
Foth, C, Tischlinger, H and Rauhut, OWM (2014) New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature 511, 79–82.Google Scholar
Fukunaga, M, et al. (2000) Molecular phylogenetic analysis of ixodid ticks based in the ribosomal DNA spacer, internal transcribed spacer 2, sequences. Journal of Parasitology 86, 38–43.Google Scholar
Geevarghese, G and Mishra, AC (2011) Haemaphysalis Ticks of India. New Delhi: ICMR, 260 pp.Google Scholar
Grimaldi, DA, Engel, MS and Nascimbene, PC (2002) Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. American Museum Novitates 3361, 1–71.Google Scholar
Guglielmone, AA and 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, 1–256.Google Scholar
Guglielmone, AA, et al. (2010) The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa 2528, 1–28.Google Scholar
Guglielmone, AA, et al. (2014) The Hard Ticks of the World (Acari: Ixodida: Ixodidae). Berlin: Springer.Google Scholar
Guglielmone, AA, et al. (2017) Genera, subgenera, species and subspecies of hard ticks (Acari: Ixodidae) described, named, renamed or given new rank by Paul Schulze (1887–1949) and their current status. Zootaxa 4325, 1–66.Google Scholar
Hoogstraal, H (1965) Phylogeny of Haemaphysalis ticks. Proceedings of the 12th International Congress of Entomology (London, July, 1964), pp. 760–761.Google Scholar
Hoogstraal, H (1969) Haemaphysalis (Alloceraea) kitaokai sp. n. of Japan, and keys to species in the structurally primitive subgenus Alloceraea Schulze of Eurasia (Ixodoidea, Ixodidae). Journal of Parasitology 55, 211–221.Google Scholar
Hoogstraal, H (1985) Argasid and nuttalliellid ticks as parasites and vectors. Advances in Parasitology 24, 135–238.Google Scholar
Hoogstraal, H and Aeschlimann, A (1982) Tick-host specificity. Bulletin de la Société Entomologique Suisse 55, 5–32.Google Scholar
Hoogstraal, H and Kim, KC (1985) Tick and mammal coevolution, with emphasis on Haemaphysalis. In Kim, KC (ed.). Coevolution of Parasitic Arthropods and Mammals. New York: John Wiley & Sons, pp. 505–568.Google Scholar
Hoogstraal, H and Wilson, N (1966) Studies on southeast Asian Haemaphysalis ticks (Ixodoidea, Ixodidae). H. (Alloceraea) vietnamensis sp. n., the first structurally primitive haemaphysalid recorded from southern Asia. Journal of Parasitology 52, 614–617.Google Scholar
Horak, IG, et al. (2012) Natural hosts of the larvae of Nuttalliella sp. (N. namaqua?) (Acari: Nuttalliellidae). Onderstepoort Journal of Veterinary Research 79(405), 1–2.Google Scholar
Huang, D, et al. (2012) Diverse transitional giant fleas from the Mesozoic era of China. Nature 483, 201–204.Google Scholar
Hugall, AF, Foster, R and Lee, MSY (2007) Calibration choice, rate smoothing, and the pattern of tetrapod diversification according to the long nuclear gene RAG-1. Systematic Biology 56, 543–563.Google Scholar
Jones, MEH, et al. (2013) Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara). BMC Evolutionary Biology 13, 208.Google Scholar
Kahn, MH, Naithani, RC and Singh, KS (1982) Study on the binomics of Nosomma monstrosum (Nutall and Warburton) (Acari: Ixodidae). Acarologia 23, 119–123.Google Scholar
Kaufman, TS (1972) A revision of the genus Aponomma Neumann, 1899 (Acarina: Ixodidae). Unpublished Ph.D. Dissertation Thesis. University of Maryland, p. 389.Google Scholar
Keirans, JE, et al. (1976) Discovery of Nuttalliella namaqua Bedford (Acarina: Ixodoidea: Nuttalliellidae) in Tanzania and redescription of the female based on scanning electron microscopy. Annals of the Entomological Society of America 69, 926–932.Google Scholar
Keirans, JE, King, DR and Sharrad, RD (1994) Aponomma (Bothriocroton) glebopalma, n. subgen., n. sp., and Amblyomma glauerti n. sp. (Acari: Ixodida: Ixodidae), parasites of monitor lizards (Varanidae) in Australia. Journal of Medical Entomology 31, 132–147.Google Scholar
Klompen, H and Grimaldi, D (2001) First Mesozoic record of a parasitiform mite: a larval argasid tick in Cretaceous amber (Acari: Ixodida: Argasidae). Annals of the Entomological Society of America 94, 10–15.Google Scholar
Klompen, JSH, et al. (1996) Evolution of ticks. Annual Review of Entomology 41, 141–161.Google Scholar
Klompen, JSH, et al. (1997) A re-evaluation of relationships in the Metastriata (Acari: Parasitiformes: Ixodidae). Systematic Parasitology 38, 1–24.Google Scholar
Klompen, JSH, et al. (2000) Systematics and biogeography of hard ticks, a total evidence approach. Cladistics 16, 79–102.Google Scholar
Klompen, JSH, Dobson, SJ and Barker, SC (2002) A new subfamily, Bothriocrotoninae n. subfam., for the genus Bothriocroton Keirans, King & Sharrad, 1994 status amend. (Ixodida: Ixodidae), and the synonymy of Aponomma Neumann, 1899 with Amblyomma Koch, 1844. Systematic Parasitology 53, 101–107.Google Scholar
Kolonin, GV (2009) Fauna of ixodid ticks of the world. Available at http://www.kolonin.org/ (August 24, 2009) (Accessed 11 July 2017).Google Scholar
Latif, AA, et al. (2012) Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): first description of the male, immature stages and re-description of the female. PLoS ONE 7(7), e41651.Google Scholar
Luo, ZX, et al. (2011) A Jurassic eutherian mammal and divergence of marsupials and placentals. Nature 476, 442–445.Google Scholar
Madder, M, Horak, I and Stoltz, H (2010) Ticks. Tick Identification. Pretoria, South Africa: University of Pretoria, Faculty of Veterinary Science, 58 pp.Google Scholar
Manilla, G (1998) Fauna d'Italia, Acari, Ixodida, Bologna: Edizioni Calderini, 280 pp.Google Scholar
Mans, BJ, et al. (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.Google Scholar
Mans, BJ, et al. (2012) The mitochondrial genomes of Nuttalliella namaqua (Ixodoidea: Nuttalliellidae) and Argas africolumbae (Ixodoidea: Argasidae): estimation of divergence dates for the major tick lineages and reconstruction of ancestral blood-feeding characteristics. PLoS ONE 7(11), e4946.Google Scholar
Mans, BJ, et al. (2016) Ancestral reconstruction of tick lineages. Ticks and Tick-borne Diseases 7, 509–535.Google Scholar
Matthee, CA and Davis, SK (2001) Molecular insights into the evolution of the family Bovidae: a nuclear DNA perspective. Molecular Biology and Evolution 18, 1220–1230.Google Scholar
Modesto, SP, et al. (2015) The oldest parareptile and the early diversification of reptiles. Proceedings of the Royal Society B 282, 20141912.Google Scholar
Müller, J and Reisz, R (2005) Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. BioEssays 27, 1069–1075.Google Scholar
Nicholson, WL, et al. (2009) Ticks (Ixodida). In Mullen, GR and Durden, LA (eds). Medical and Veterinary Entomology, 2nd edn. New York: Academic Press, pp. 493–542.Google Scholar
Norman, JE and Ahsley, MV (2000) Phylogenetics of Perissodactyla and tests of the molecular clock. Journal of Molecular Evolution 50, 11–21.Google Scholar
Nuttall, GHF and Warburton, C (1915) Ticks. A Monograph of the Ixodida. Part III. The Genus Haemaphysalis. London: Cambridge University Press, pp. 349–550.Google Scholar
Peñalver, E, et al. (2017) Ticks parasitized feathered dinosaurs as revealed by Cretaceous amber assemblages. Nature Communications, 8, 1924.Google Scholar
Perez-Eid, C (2007) Les tiques. Identification, biologie, importance medicale et veterinaire. Ed. Lavoisier, 278 pp.Google Scholar
Pereira, SL and Baker, AJ (2006) A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock. Molecular Biology and Evolution 23, 1731–1740.Google Scholar
Phillips, MJ, Bennett, TH and Lee, MSY (2009) Molecules, morphology, and ecology indicate a recent, amphibious ancestry for echidnas. Proceedings of the National Academy of Science of the USA 106, 17089–17094.Google Scholar
Poinar, GO Jr, (1995) First fossil soft tick, Ornithodoros antiquus n. sp. (Acari: Argasidae) in Dominican amber with evidence of their mammalian host. Experimentia Basel 51, 584–587.Google Scholar
Poinar, GO Jr, and Brown, AE (2003) A new genus of hard ticks in Cretaceous Burmese amber (Acari: Ixodida: Ixodidae). Systematic Parasitology 54, 199–205.Google Scholar
Poinar, GO Jr, and Buckley, R (2008) Compluriscutula vetulum (Acari: Ixodida: Ixodidae), a new genus and species of hard tick from Lower Cretaceous Burmese amber. Proceedings of the Entomological Society of Washington 110, 445–450.Google Scholar
Prum, RO (1999) Development and evolutionary origin of feathers. Journal of Experimental Zoology 285, 291–306.Google Scholar
Prum, RO, et al. (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573.Google Scholar
Reisz, RR and Fröbisch, J (2014) The oldest caseid synapsid from the Late Pennsylvanian of Kansas, and the evolution of herbivory in terrestrial vertebrates. PLoS ONE 9(4), e94518.Google Scholar
Ross, AJ (2017) Burmese (Myanmar) amber taxa, on-line checklist v. 2017.4. 88pp. Available at http://www.nms.ac.uk/explore/stories/natural-world/burmese-amber/.Google Scholar
Ross, A, et al. (2010) Burmese amber. In Penney, D (ed.). Biodiversity of Fossils in Amber from the Major World Deposits. Manchester: Siri Scientific Press, pp 208–235.Google Scholar
Rubidge, BS and Sidor, CA (2001) Evolutionary patterns among Permo–Triassic therapsids. Annual Review of Ecology and Systematics 32, 449–480.Google Scholar
Sands, AF, et al. (2017) Effects of tectonics and large scale climatic changes on the evolutionary history of Hyalomma ticks. Molecular Phylogeny and Evolution 114, 153–165.Google Scholar
Schachat, SR, Robbins, RG and Goddard, J (2018) Color patterning in hard ticks (Acari: Ixodidae). Journal of Medical Entomology 55, 1–13.Google Scholar
Schulze, P (1942) Die Gestaltung der Mitteldarmes bei den Zecken und die Einrichtungen für die Körperdehnung bei der Blutaufnahme (nebst Beiträgen zur Lebensgeschichte der Ixodoidea). Zeitschrift für Morphologie und Ökologie der Tiere 39, 320–368.Google Scholar
Selden, PA and Ren, D (2017) A review of Burmese amber arachnids. Journal of Arachnology 45, 324–343.Google Scholar
Shi, G-H, et al. (2012) Age constraints on Burmese amber based on U–Pb dating of zircons. Cretaceous Research 37, 155–163.Google Scholar
Simmons, NB, et al. (2008) Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–821.Google Scholar
Smith, MW (1973) The effect of immersion in water on the immature stages of the ixodid ticks-Rhipicephalus appendiculatus (Neumann 1901) and Amblyomma variegatum (Fabricus 1794). Annals of Tropical Medicine and Parasitology 67, 483–492.Google Scholar
Smith, VS, et al. 2011. Multiple lineages of lice pass through the K–Pg boundary. Biology Letters 7, 782–785.Google Scholar
Smithson, TR, et al. (2012) Earliest Carboniferous tetrapod and arthropod faunas from Scotland populate Romer's Gap. Proceedings of the National Academy of Science of the USA 109, 4532–4537.Google Scholar
Sonenshine, D. and Roe, RM, (eds) (2013) Biology of Ticks, 2nd edn. Bands 1–2. Oxford: Oxford University Press.Google Scholar
Teeling, EC, et al. (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307, 580–584.Google Scholar
Theodor, JM (2004) Molecular clock divergence estimates and the fossil record of Ceratiodactyla. Journal of Paleontology 78, 39–44.Google Scholar
Weidner, H (1964) Eine Zecke, Ixodes succineus sp. n., im baltischen Bernstein. Veröffentlichungen aus dem Überseemuseum Bremen 3, 143–151.Google Scholar
Williamson, TE, Brusatte, SL and Wilson, GP (2014) The origin of metatherian mammals: the Cretaceous record. ZooKeys 465, 1–76.Google Scholar
Zumpt, F (1951) Phylogenie der Zecken und ‘Natürliches System’. Zeitschrift für Parasitenkunde 15, 87–101.Google Scholar