- Research article
- Open Access
Microtomography of the Baltic amber tick Ixodes succineus reveals affinities with the modern Asian disease vector Ixodes ovatus
BMC Evolutionary Biology volume 16, Article number: 203 (2016)
Fossil ticks are extremely rare and Ixodes succineus Weidner, 1964 from Eocene (ca. 44–49 Ma) Baltic amber is one of the oldest examples of a living hard tick genus (Ixodida: Ixodidae). Previous work suggested it was most closely related to the modern and widespread European sheep tick Ixodes ricinus (Linneaus, 1758).
Restudy using phase contrast synchrotron x-ray tomography yielded images of exceptional quality. These confirm the fossil’s referral to Ixodes Latreille, 1795, but the characters resolved here suggest instead affinities with the Asian subgenus Partipalpiger Hoogstraal et al., 1973 and its single living (and medically significant) species Ixodes ovatus Neumann, 1899. We redescribe the amber fossil here as Ixodes (Partipalpiger) succineus.
Our data suggest that Ixodes ricinus is unlikely to be directly derived from Weidner’s amber species, but instead reveals that the Partipalpiger lineage was originally more widely distributed across the northern hemisphere. The closeness of Ixodes (P.) succineus to a living vector of a wide range of pathogens offers the potential to correlate its spatial and temporal position (northern Europe, nearly 50 million years ago) with the estimated origination dates of various tick-borne diseases.
Ticks (Acari: Ixodida) are iconic arachnids, being obligate ectoparasites of vertebrates and often of considerable economic significance as disease vectors affecting humans and/or domestic animals. For a recent summary of their biology see Sonenshine & Roe . Almost 900 living species of ticks in three families (Nutalliellidae, Argasidae and Ixodidae) are currently recognized  and their origins and evolution remain a topic of debate [3–5]. Key questions include whether ticks share a common ancestor with mesostigmatid mites – or a lineage thereof  – or alternatively with the large and rare holothyrid mites . Second, when did ticks originate, given that modern taxa require terrestrial vertebrate hosts, and on which palaeocontinent did they first appear? Recent opinions include an inferred Gondwanan (specifically South African) origin , in the Permian, although the same authors subsequently preferred an East African origin in the Carboniferous . Other data suggest Australia, perhaps as far back as the Devonian . Finally what, therefore, were their initial hosts? The monotypic and probably basal family Nutalliellidae has been reported as feeding on lizards , but was later shown to be a more generalist parasite  with, for example, subadults found on mammals like elephant shrews . Note that tortoises, mammal-like reptiles, birds, and perhaps even feathered dinosaurs, would have been possible hosts for at least the Mesozoic species.
Palaeontology has the potential to contribute to this debate by recording when and where particular lineages (families, genera) were present. The oldest acariform mites are Devonian, but the oldest parasitiform mites – the clade which includes the ticks – have only been recorded since the Cretaceous. Fossil ticks are extremely rare. The oldest are two hard tick species (Ixodidae) from the Cretaceous (ca. 99 Ma) Burmese amber from Myanmar [13, 14]. Both were assigned to extinct genera; albeit not by recognized tick specialists. Burmese amber also includes a report of the living genus Amblyomma (Klompen in ), but was not described at species level. Like this find, all other fossil ticks have been assigned to extant genera, implicit of a strong degree of morphological stasis. The next oldest record is a soft tick (Argasidae: Carios) from Cretaceous (ca. 92 Ma) New Jersey amber . This is followed by an Ixodes from Eocene (ca. 44–49 Ma) Baltic amber , which forms the focus of the present study, as well as a record of Hyalomma from Baltic amber , albeit without formal description. A putative Ixodes from the contemporary Green River Formation of Wyoming, USA is a nomen dubium . Miocene (ca. 16 Ma) Dominican Republic amber has yielded an extinct species of the soft tick Ornithodoros , plus two hard ticks effectively indistinguishable from living Neotropical Ambylomma species [20, 21]. The youngest records are subfossils (<1 Ma) and include a Dermacentor from the ear of a fossilized rhinoceros from Poland (Kulczyński in ) and an Ixodes in an ancient owl pellet from Argentina . In both cases the specimens could be comfortably assigned to living species.
Ixodes succineus Weidner, 1964 from Baltic amber (Fig. 1) is thus of particular significance as one of the oldest putative records of a living hard tick genus. We should also stress that numerous Ixodes species act as disease vectors today, thus understanding the origins of the genus is of wider parasitological interest. Including the amber fossil, Guglielmone et al.  recognized 244 valid Ixodes species and noted [see also 2] the, to some extent controversial , attempts to split the genus into subtaxa. The monophyly of Ixodes is by no means certain and a broad division into an Australasian and a non-Australasian clade has been proposed . So where does the amber fossil fit into this scheme? Baltic amber is obviously geographically from northern Europe, but has been shown to occasionally pick up Asian or even Gondwanan faunal elements. Yet both the original description of I. succineus  and subsequent commentaries  remarked on similarities between the amber fossil and the common, Recent, largely European species Ixodes ricinus Linneaus, 1758; often known as the sheep, deer or castor bean tick. Ixodes succineus has been mentioned in tick catalogues  and refigured in popular works on amber [28–30], but a modern restudy of this important inclusion is lacking.
Fossils can be useful in constraining times of cladogenesis by acting as calibration points for molecular clocks [31, 32]. However, this requires accurate taxonomic placement, which in turn is facilitated by techniques which maximize the amount of morphological data recovered and allow the fossils to be placed using the same character sets as those applied to living genera and species. In recent years various forms of computed tomography (CT) have proved particularly well suited for imaging inclusions in amber, and have been successfully applied in acarology to both oribatid  and astigmatid mites . Here, we offer the first CT study of a tick in amber. As well as producing extremely high-quality images of the inclusion (Fig. 2), our principal aim was to assess the fossil’s affinities – specifically is it an Ixodes and if so how close is it to Ixodes ricinus or to other living species? As noted above, Ixodes ticks often transmit diseases. Confirming the identity of the fossil would also allow us to compare this Eocene record with estimates of origination dates for pathogens typically carried by closely-related living tick species.
The holotype and only specimen of Ixodes succineus derives from the legacy of a Baltic amber collection owned by the former physiology professor Otto Weiss (1871–1943) in Königsberg (now the Kaliningrad Oblast, Russia). It was purchased by the Überseemuseum Bremen, Germany in the early 1960s . The geoscientific portion of this museum was transferred to the University of Bremen in 1994, thus the specimen is now held in the ‘Geowissenschaftliche Sammlung’ of the university under the inventory number GSUB I21. Baltic amber is conventionally dated to an Eocene (Lutetian) age of ca. 44–49 Ma and is thought to have been deposited in a warm forest environment . The fossil was also examined under a stereomicroscope and compared both to Recent species held in the United States National Tick Collection and the literature.
Microtomographic data were collected at the bending magnet beam line 2-BM at the Advanced Photon Source, Argonne National Laboratory, USA. The amber specimen was scanned with 27.2 keV x-ray and imaged with a lens-coupled x-ray microscope. The microscope is composed of a Coolsnap K4 2048 × 2048 CCD camera, a 100um LuAG:Ce scintillator, and a Zeiss 5× objective lens. The scintillator converts the amber x-ray shadow image into an optical image, and the objective lens projects the image onto the camera. The microscope has a 2.96 μm pixel size. The exposure time was 200 ms. images were collected in transmission mode by a CCD camera behind the sample in the hutch configuration. The sample-detector distance was set to 300 mm to optimize the phase contrast which was needed to illustrate internal details of the poorly absorbing specimen; this distance being based on the evolution of the contrast in the reconstructed images. 1440 projections were acquired while the sample was rotated over 180° in steps of 0.125°. A microtomographic data set with a size of 2048x2048x1949 voxels (voxel size 2.96 μm) was reconstructed using a phase retrieval algorithm . Digital visualization was achieved using ZIBAmira (https://amira.zib.de/). Synchrotron x-ray tomography techniques are known to run the risk of darkening the amber matrix surrounding the specimen, however no noticeable darkening was observed using the parameters listed above.
Suborder IXODIDA Leach, 1815
Family IXODIDAE Leach, 1815
Genus Ixodes Latreille, 1795
Ixodes (Partipalpiger) succineus Weidner, 1964
Horizon and locality
Baltic amber, probably from the Kaliningrad region, Eocene (Lutetian).
Extinct member of the subgenus Partipalpiger Hoogstraal, Clifford, Saito & Keirans, 1973, which can be distinguished from the single living species by a 3/3 dental formula on almost the entire hypostome (2/2 in Ixodes ovatus Neumann, 1899) and a moderately long posteromedian spur on coxae I (short in Ixodes ovatus).
Female tick. Idiosoma (Figs. 2 and 3): suboval, widest at level of coxae IV; length from scapular apices to posterior body margin 0.86 mm, breadth 0.56 mm, 1.54 times as long as broad. Scutum (Fig. 2b): Elongate, outline broadly rounded, length 0.64 mm, width 0.47 mm, 1.36 times as long as broad. Lateral carinae distinct, divergent, not reaching posterior margin; cervical grooves indistinct, shallow. Genital aperture medial to posterior margin of coxae IV; genital apron lacking. Genital groove well-developed. Anal groove circular with open posterior margin. Spiracular plates (Fig. 2b): sub-circular; diameter in anteroposterior plane slightly greater than that in dorsoventral plane; length 0.10 mm, width 0.09 mm, 1.11 times as long as broad.
Gnathosoma (Fig. 2d): length from palpal apices to cornual apices dorsally 0.34 mm, width at apices of lateral projections 0.23 mm, 1.48 times as long as broad. Basis capituli (Fig. 2b): dorsally subtriangular; posterior margin nearly straight; cornua small. Basis capituli ventrally pentagonal; with posterior margin convex; auriculae absent. Palpi (Fig. 2d): elongate, narrow; length (I–III segments) 0.26 mm, width 0.08 mm, 3.25 times as long as broad, length of segments in descending order: 2, 3, 1, 4; segment I well developed without spurs; segment II narrow proximally and gradually widening to mid-length and nearly parallel sided from mid-length to distal end; segment III laterally straight and medially converging to bluntly rounded apex. Hypostome (Fig. 2d): tapering with sharply pointed apex; arising from a medial anterior extension of basis; length 0.17 mm, width 0.05 mm, 3.4 times as long as broad; widest nearly at midlength; dental formula 3/3 throughout hypostomal length; denticles sharply pointed.
Legs: moderately long, slender. Coxae (Fig. 2e): coxae I with moderately long triangular posteromedian spur with sharply pointed apex, posterolateral spur lacking; coxae II without spurs; coxae III and IV with short triangular spur with blunt apex; coxae I–II with syncoxae; syncoxae on coxae II large, occupying posterior half of coxae. Tarsi (Fig. 2a): tarsi I–IV not humped at distal end; tarsus I length 0.22 mm; tarsus IV length 0.19 mm. Male, nymph and larva unknown.
GSUB I21 can be confirmed here both as a female fossil tick, and as the oldest unequivocal record of Ixodes. Based on the presence of syncoxae on coxae I and II (Figs. 2 and 3), the female of I. succineus most closely resembles members of the subgenera Afrixodes Morel, 1966, Exopalpiger Schulze, 1935 (including Endopalpiger Schulze, 1935), Ixodes s. str. and Partipalpiger. Species belonging to the Afrixodes subgenus – mostly distributed in the Afrotropical region and with a few species present in the Oriental region – have syncoxae present on coxae I–III and a genital apron. By contrast, the female of I. succineus has no syncoxae on coxae III and we were unable to find any trace of a genital apron. Most species of the subgenus Exopalpiger, mostly distributed in Australasian and Neotropical regions with a few species present in the Palaearctic and Afrotropics, also have coxae III and IV with syncoxae, no spurs on any coxae and palpal segment I with large projections. The female of I. succineus has syncoxae only on coxae I and II, a well-developed posteromedian spur on coxae I and posterolateral spurs on coxae III and IV, and a palpal segment I without large projections (Figs. 2 and 3).
Females of a number of species of the subgenus Ixodes s. str. also have syncoxae on coxae I and II only. These species can be found in the Palearctic, Oriental, Nearctic and Neotropical zoogeographic regions and probably do not form a natural group (see Discussion). We examined all valid species of Ixodes s. str. and were unable to find a modern species with a combination of characters exactly matching those in the amber fossil. In Ixodes s. str. species the syncoxae are considerably narrower and many of them have a posterolateral spur present on coxae II and/or larger and longer auriculae. By contrast, the female of I. succineus has very broad syncoxae on coxae II, no spurs on coxae II and very short and blunt auriculae (Figs. 2 and 3). It is the subgenus Partipalpiger – containing only Ixodes ovatus and distributed in the Palaearctic and Oriental regions from the Himalayas to Japan – which expresses a morphology most similar to the fossil in amber. Females of I. ovatus also have syncoxae only on coxae I and II and the syncoxae on coxae II are broad, occupying the posterior half of the coxae. Both the fossil and the extant species have very short, blunt auriculae with their apices oriented laterally. Nevertheless females of Ixodes ovatus can be easily distinguished from that of I. succineus by a 2/2 dental formula on almost the entire hypostome, as opposed to 3/3 in I. succineus, and a short posteromedian spur on coxae I, which is moderately long in I. succineus (Figs. 2 and 3).
Weidner’s original suggestion  that Ixodes succineus is closest to Ixodes ricinus could not be confirmed. It seems unlikely that this common, Recent, European species is derived directly from the lineage containing the Baltic amber inclusion. We see no obvious morphological continuum from the fossil to the Ixodes species which inhabits the Baltic region today. The evolutionary origins of the modern sheep tick must be sought elsewhere, and in any case these ectoparasites must surely have immigrated into north–central Europe after the last glaciation. Among recent molecular phylogenies of Ixodes [26, 36–38] it is worth noting the proposal that the genus is not monophyletic , and that ixodid ticks in general originated either in Africa or Australia. Our data confirms that Ixodes had reached Europe by at least 49 Ma. Furthermore, Xu et al.  challenged the monophyly of the Ixodes ricinus species complex and suggested that these ticks underwent – at some stage – a rapid radiation. Perhaps this was associated with the availability of their mammalian hosts. Further studies are undoubtedly needed to unravel the history of the modern European Ixodes tick fauna, and fossils could be integral to this process. As has been argued for insects , resolving phylogenies associated with rapid radiations in deep time can be problematic. Amber fossils like Ixodes succineus can take on increased importance for deciphering the phylogeny of rapidly-radiating groups, as they can reflect extinct lineages which sample different portions of the original radiation.
Our microtomography results suggest instead that Ixodes succineus from Baltic amber is most closely related to a modern Asian species, Ixodes ovatus, and can potentially be assigned to the same subgenus, Partipalpiger. This in itself is interesting and suggests that around 50 million years ago the Partipalpiger lineage (or at least closely-related forms) was more widespread across the northern hemisphere but became, at some stage, extinct in Europe. Partipalpiger has been resolved as the sister group of the subgenus Ixodes (s. str.)  and if this is correct the latter subgenus must also date back at least ca. 50 Ma. We may note here the proposal of Filippova  that Ixodes (s. str.) dates back to the Palaeogene, with an ecological niche in mesophilic and moderately hydrophilic Cenozoic forests. An open question is whether the loss of lineages, i.e., Partipalpiger, from the Eocene of northern Europe also occurred tens of millions of years ago, or perhaps as recently as the Pliocene–Quaternary Ice Ages which began about ca. 2.6 Ma. Baltic amber is thought to have concurred with a warm period – the Paleocene–Eocene Thermal Maximum and Early Eocene Climatic Optimum – and is known to host a range of taxa now restricted to other biogeographical areas. Larsson  reviewed Baltic amber fossils belonging to lineages which survive today either in southern Africa or in Asia. We propose that Ixodes succineus can be added to the latter group. Another example among parasitiform mites would be the opilioacarid genus Paracarus which has been recorded from Baltic amber , but is found today only in Kazakhstan.
Correlations with pathogen origins?
In a wider context, Poinar  reviewed a number of insects in amber – particularly mosquitos, sand flies and assassin bugs – which today carry medically significant pathogens, and in which these exceptionally preserved inclusions even retained direct evidence for the protozoans responsible for infection. In a similar vein, Poinar  claimed to have observed rickettsial-like bacteria in one of the Burmese amber ticks, implying a minimum age of ca. 99 million years for this host–bacterial association. Whether these structures are genuine internal features or, e.g., an artefact of a reticulate surface ornament under particular conditions of illumination needs to be checked against the original material. This was, unfortunately, not available for loan. Potential pathogens cannot be resolved in our Baltic amber tick, but like a number of Ixodes species, its closest living relative I. ovatus is medically significant. For a detailed account of its biology see Hoogstraal et al. . Ixodes ovatus has been recorded as a vector for the Borellia spirochetes responsible for Lyme borreliosis (LB) , for the Babesia protozoans responsible for babesiosis [47, 48], the bacteria responsible for anaplasmosis, ehrlichiosis and rikettsia-related infections [49, 50], and for the tick-borne encephalitis virus (TBEV) .
It is thus interesting to speculate whether the closely-related amber species was also a significant (mammalian) disease vector? Mammals, of course, underwent an adaptive radiation in the aftermath of the end-Cretaceous mass extinction. De la Fuente et al.  reviewed the role of (living) ticks as vectors, and our present revision of Ixodes (P.) succineus places a potential host in the Eocene of Europe. It may be instructive to compare this date to estimates of origination for the protozoa, bacteria or viruses which are intimately associated either with Ixodes, or with hard ticks in general. For example, Florin-Christensen & Schnittiger  discussed the evolutionary history of piroplasmids (including Babesia) and ticks. Molecular clock data suggests that piroplasmids in general originated ca. 57 Ma – i.e., just prior to the age of our fossil – but that the radiation into subgroups, including the babesids, is somewhat younger: ca. 25 Ma. Taking the oldest Mesozoic ticks as a starting point, these authors suggested that piroplasmids presumably entered a tick host at some point between the Cretaceous and the Oligocene.
Lyme disease is strongly associated with Ixodes species today, although it remains to be resolved whether the spirochetes entered ticks only once, or on multiple occasions. As reviewed by Fukunaga et al.  the phylogeny of the Borellia pathogen responsible is quite concordant with the phylogeny of the Ixodes ticks which host them: for example I. ovatus today hosts B. japonica. When the ticks, and their pathogens, radiated is another question. Margos et al.  noted that a molecular clock for the evolution of the housekeeping genes of the causative agent in humans, B. burgdorferi – which is strongly associated with the I. ricinus complex – has not yet been established. Nevertheless, these authors suggested that its origins were in Europe and that various lineages of this pathogen may have separated a few (unspecified) millions of years ago. The TBEV virus may also be a fairly recent acquisition. It has been hypothesised that these flaviviruses crossed over from argasid ticks on seabirds into ixodid ticks in modern Eurasian forests, or that its emergence may be associated with climate change at the end of the last glaciation .
Further data is available for bacterial infections [55, 56] and both studies inferred a Jurassic–Cretaceous split into Rickettsia bacteria associated with protozoans and a lineage more typical for hematophagous arthropods. This would be consistent with Poinar’s Burmese amber tick record (ca. 99 Ma) and his putative Rickettsia-like inclusions. Interestingly, both these Rickettsia molecular studies also reported a rapid radiation of this bacterial genus among blood-feeding taxa going back to ca. 50–65 Ma; more or less contemporary with the Baltic amber fossil but also, of course, with a radiation of possible mammalian hosts. Similarly, two medically significant strains of Anaplasma (A. marginale and A. phagocytophilum) were dated  as having split ca. 43–78 Ma.
We cannot prove that Ixodes succineus carried bacteria, or other pathogens, but our study does confirm that at least one anatomically modern species of Ixodes was already present during the Eocene. It is closely related to a modern disease vector and can be placed in the same subgenus (Partipalpiger) as the Asian tick Ixodes ovatus. Thus the amber fossil may have acted as a vector too. Molecular estimates of origination dates suggest that at least piroplasmids and the Rickettsia and Anaplasma bacteria should have been present around 50 million years ago as well. This begs a further question whether evolution and radiation events among the pathogens are more closely tied to the ticks – as one of their carriers – or to the mammals as their principal hosts and reservoirs.
Sonenshine D, Roe RM. (editors) Biology of Ticks, 2nd Edition. Bands 1–2. Oxford: Oxford Univ. Press; 2013.
Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG, Shao R, Barker SC. The Argasidae, Ixodidae and Nutalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa. 2010;2528:1–28.
Klompen JSH, Black IV WC, Keirans JE, Oliver Jr JH. Evolution of ticks. Annu Rev Entomol. 1996;41:141–61.
Baker SC, Murrell A. Phylogeny, evolution and historical zoogeography of ticks: a review of recent progress. Exp Appl Acarol. 2002;28:55–68.
De la Fuente J. The fossil record and the origin of ticks (Acari: Parasitiformes: Ixodida). Exp Appl Acarol. 2003;29:331–44.
Karg W, Schorlemmer A. Origin and classification of the Ixodides (ticks) within the Parasitiformes Reuter 1909 (Acarina). Acarologia. 2008;48:123–34.
Klompen H. Holothyrids and ticks: new insights from larval morphology and DNA sequencing, with the description of a new species of Diplothyrus (Parasitiformes: Neothyridae). Acarologia. 2010;50:269–85.
Mans BJ, de Klerk D, Pienaar R, Latif AA. Nuttalliella namaqua: a living fossil and closest relative to the ancestral tick lineage: implications for the evolution of blood-feeding in ticks. PLoS One. 2011;6(8):e23675.
Mans BJ, de Klerk D, Pienaar R, Castro MH, Latif AA. 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. 2012;7(11):e4946.
Barker SC, Walker AR, Campelo D. A list of 70 species of Australian ticks; diagnostic guides to and species account 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. Int J Parasitol. 2014;44:941–53.
Mans BJ, de Klerk D, Pienaar R, Latif AA. The host preferences of Nuttalliella namaqua (Ixodoidea: Nuttalliellidae): a generalist approach to surviving multiple host-switches. Exp Appl Acarol. 2014;62:233–40.
Hoffmann S, Horak IG, Bennett NC, Lutermann H. Evidence for interspecific interactions in the ectoparasite infracommunity of a wild mammal. Parasit Vectors. 2016;9(58):1–11.
Poinar Jr GO, Brown AE. A new genus of hard ticks in Cretaceous Burmese amber (Acari: Ixodida: Ixodidae). Syst Parasitol. 2003;54:199–205.
Poinar Jr GO, Buckley R. Compluriscutula vetulum (Acari: Ixodida: Ixodidae), a new genus and species of hard tick from Lower Cretaceous Burmese Amber. Proc Entomol Soc Wash. 2008;110:445–50.
Grimaldi DA, Engel MS, Nascimbene PC. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am Mus Novit. 2002;3361:1–71.
Klompen H, Grimaldi D. First Mesozoic record of a parasitiform mite: a larval argasid tick in Cretaceous amber (Acari: Ixodida: Argasidae). Ann Entomol Soc Am. 2001;94:10–5.
Weidner H. Eine Zecke, Ixodes succineus sp. n., im baltischen Bernstein. Veröffent Übersee-Mus Bremen. 1964;3:143–51.
Dunlop JA. The fate and status of the supposed fossil tick Ixodes tertiarius Scudder, 1885. Acarologia. 2011;51:399–404.
Poinar Jr GO. First fossil soft tick, Ornithodoros antiquus n. sp. (Acari: Argasidae) in Dominican amber with evidence of their mammalian host. Experimentia Basel. 1995;51:584–7.
Lane RS, Poinar Jr GO. First fossil tick (Acari: Ixodidae) in New World amber. Int J Acarol. 1986;12:75–8.
Keirans JE, Lane RS, Cauble R. A series of larval Amblyomma species (Acari : Ixodidae) from amber deposits in the Dominican Republic. Int J Acarol. 2002;28:61–6.
Schille F. Entomologie aus der Mammut- und Rhinoceros-Zeit Galiziens. Entomol Z. 1916;30:42–3.
Sanchez JP, Nava S, Lareschi M, Ortiz PE, Guglielmone AA. Finding of an ixodid tick inside a Late Holocene owl pellet from northwestern Argentina. J Parasitol. 2010;96:820–2.
Guglielmone AA, Nava S. 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. 2014;3767:1–256.
Camicas JL, Hervy J-P, Adam F, Morel PC. Les tiques du monde. Nomenclature, stades décrits, hôtes, répartition (Acarida, Ixodida). Paris: Orstom; 1998.
Klompen JSH, Black IV WC, Keirans JE, Norris DE. Systematics and biogeography of hard ticks, a total evidence approach. Cladistics. 2000;16:79–102.
Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. Comments on controversial tick (Acari: Ixodida) species names and species described or resurrected from 2003 to 2008. Exp Appl Acarol. 2009;48:311–27.
Weitschadt W. Zecken im Bernsteinwald – wahre Raritäten. ImpfDialog. 2004;4:11–2.
Wichard W, Weitschat W. Im Bernsteinwald. Gebrüder Gerstenberg: Hildersheim; 2005.
Lehmann J. Fossile Zecke im baltischen Bernstein. Fossilien. 2007;24:226–8.
Florin-Christensen M, Schnittiger L. Piroplasmids and ticks: a long-lasting intimate relationship. Front Biosci. 2009;14:3064–73.
Gou H, Guan G, Liu A, Ma M, Chen Z, Ren Q, Li Y, Yang J, Yin H, Luo J. Coevolutionary analyses of the relationships between piroplasmids and their hard tick hosts. Ecol Evol. 2013;3:2985–93.
Heethoff M, Helfen L, Norton RA. Description of Neoliodes dominicus n. sp. (Acari, Oribatida) from Dominican amber, aided by synchrotron X-ray microtomography. J Paleontol. 2009;83:153–9.
Dunlop JA, Wirth S, Penney D, McNeil A, Bradley RS, Withers PJ, Preziosi RF. A minute fossil phoretic mite recovered by phase-contrast X-ray computed tomography. Biol Lett. 2012;8:457–60.
Paganin D, Mayo SC, Gureyevte TE, Miller PR, Wilkins SW. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J Microsc. 2002;206:33–40.
Caporale DA, Rich SM, Spielman A, Telford III SR, Kocher TD. Discriminating between Ixodes ticks by means of mitochondrial DNA sequences. Mol Phylogenet Evol. 1995;4:361–5.
Fukunaga M, Yabuki M, Hamase A, Oliver Jr JH, Nakao M. Molecular phylogenetic analysis of ixodid ticks based on the ribosomal DNA spacer, internal transcribed spacer 2, sequences. J Parasitol. 2000;86:38–43.
Xu G, Fang QQ, Keirans JE, Durden LA. Molecular phylogenetic analyses indicate that the Ixodes ricinus complex is a paraphyletic group. J Parasitol. 2003;89:452–7.
Whitfield JB, Kjer KM. Ancient rapid radiations of insects: Challenges for phylogenetic analysis. Ann Rev Entomol. 2007;53:449–72.
Filippova NA. Ixodid ticks of the subfamily Ixodinae. Fauna of the USSR, Arachnida, Vol. 4, issue 4. (Nauka Publishing House, 1977).
Larsson SG. Baltic amber—a paleobiological study. Entomonograph. 1978;1:1–192.
Dunlop JA, Wunderlich J, Poinar Jr GO. The first fossil opilioacariform mite (Acari: Opilioacariformes) and the first Baltic amber camel spider (Solifugae). Trans R Soc Edinburgh: Earth Sci. 2004;94:261–73.
Poinar jr GO. The origin of insect-borne human diseases as revealed in amber. Am Entomol. 2011; Fall 2011:170–178.
Poinar Jr GO. Rikettsial-like cells in the Cretaceous tick, Cornupalpatum burmanicum (Ixodida: Ixodidae). Cret Res. 2015;52:623–7.
Hoogstraal H, Clifford CM, Saito Y, Keirans JE. Ixodes (Partipalpier) ovatus Neumann, subgen. nov. identity hosts, ecology and distribution (Ixodoidea; Ixodidae). J Med Entomol. 1973;10:157–64.
Miyamoto K, Nakao M, Uchikawa K, Fujita H. Prevalence of Lyme borreliosis spirochetes in ixodid ticks of Japan, with special reference to a new potential vector, Ixodes ovatus (Acari: Ixodidae). J Med Entomol. 1992;29:216–20.
Yano Y, Saito-Ito A, Anchalee D, Takada N. Japanese Babesia microti cytologically detected in salivary glands of naturally infected tick Ixodes ovatus. Microbiol Immunol. 2005;49:891–7.
Zamato-Niikura A, Tsuji M, Qiang W, Nakao M, Hirata H, Ishihara C. Detection of two zoonotic Babesia microti lineages, the Hobetsu and U.S. lineages, in two sympatric tick species, Ixodes ovatus and Ixodes persulcatus, respectively, in Japan. Appl Environ Microbiol. 2012;78:3424–30.
Ohashi N, Inayoshi M, Kitamura K, Kawamori F, Kawaguchi D, Nishimura Y, Naitou H, Hiroi M, Masuzawa T. Anaplasma phagocytophilum-infected ticks, Japan. Emerg Infect Dis. 2005;11:1780–3.
Munderloh UG, Silverman DJ, MacNamara KC, Ahlstrand GG, Chaterjee M, Winslow GM. Ixodes ovatus Ehrlichia exhibits unique ultrastructural characteristics in mammalian endothelial and tick-derived cells. Ann N Y Acad Sci. 2009;1166:112–9.
Takeda T, Ito T, Chiba M, Takahashi K, Niioka T, Takashima I. Isolation of tick-borne encephalitis virus from Ixodes ovatus (Acari: Ixodidae) in Japan. J Med Entomol. 1998;35:227–41.
De la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 2008;13:6938–46.
Margos G, Gatewood AG, Aanensen DM, Hanincová K, Terekhova D, Vollmer SA, Cornet M, Piesman J, Donaghy M, Bormane A, Hurn MA, Feil EJ, Fish D, Casjens S, Wormser GP, Schwartz I, Kurtenbach K. MLST of housekeeping genes captures geographic population structure and suggests a European origin of Borrelia burgdorferi. Proc Natl Acad Sci U S A. 2008;105:8730–5.
Subbotina EL, Loktev VB. Molecular evolution of tick-borne encephalitis and Powassan viruses. Mol Biol. 2012;46:75–84.
Stothard DR, Fuerst PA. Evolutionary analysis of the spotted fever and typhus groups of Rickettsia using 16S rRNA gene sequences. Syst Appl Microbiol. 1995;18:52–61.
Weinert LA, Werren JH, Aebi A, Stone GN, Jiggins FM. Evolution and diversity of Rickettsia bacteria. BMC Biol. 2009;7:6.
Foley J, Nieto NC, Foley P, Teglas MB. Co-phylogenetic analysis of Anaplasma phagocytophilum and its vectors, Ixodes spp. ticks. Exp Appl Acarol. 2008;45:155–70.
We appreciate technical support by M. Krogmann (Bremen), and thank P. Selden (Kansas) for useful discussions about fossil arachnids. R. Garwood and two anonymous reviewers provided valuable comments on the typescript. Use of the Advanced Photon Source, an Office of Science User Facility operated for the U.S. Department of Energy (DOE) Office of Science by Argonne National Laboratory, was supported by the U.S. Department of Energy under Contract No. DE-AC02-06CH11357. DAA’s part of this project was partially supported by Grant Number R15AI096317 from the National Institute of Allergy and Infectious Diseases. The content is the sole responsibility of the authors and does not necessarily represent the official views of the National Institute of Allergy and Infectious Diseases or the National Institutes of Health.
Availability of data and materials
The original holotype specimen of Ixodes succineus is available from the University of Bremen (see Methods). The video reconstruction is available as Additional file 1.
JAD and DAA wrote most of the text and descriptions, with contributions to the specimen and locality data by JL and RH. Tomographic images and the reconstruction were produced by FF, ME, SZ, XX and RH who also wrote the methods section. All authors contributed intellectually to the paper.
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
About this article
Cite this article
Dunlop, J.A., Apanaskevich, D.A., Lehmann, J. et al. Microtomography of the Baltic amber tick Ixodes succineus reveals affinities with the modern Asian disease vector Ixodes ovatus . BMC Evol Biol 16, 203 (2016). https://doi.org/10.1186/s12862-016-0777-y
- Baltic amber