Biology of Amblyomma

Following Klompen et al. (Reference Klompen, Dobson and Barker2002) the genus Aponomma Neumann, 1899 is now considered a synonym of Amblyomma, which is represented today by 132 valid, extant species (Guglielmone and Nava, Reference Guglielmone and Nava2014). In detail, Klompen et al. (Reference Klompen, Dobson and Barker2002) transferred some of the Aponomma species from the indigenous Australian Aponomma to Bothriocroton Keirans et al., 1994 and the remaining Aponomma species to Amblyomma. The genus Amblyomma is thus currently distributed in all six zoogeographic regions (Guglielmone et al. Reference Guglielmone, Robbins, Apanaskevich, Petney, Estrada-Peña and Horak2014), although we should stress that 98% of them occur exclusively or non-exclusively in territories that originally constituted Gondwana. By contrast, only three species are exclusively found in the Neartic region (Guglielmone et al. Reference Guglielmone, Robbins, Apanaskevich, Petney, Estrada-Peña and Horak2014), which was originally part of Laurasia. Typical hosts of Amblyomma today include lizards and snakes (Squamata) as well as tortoises (Testudines) which form the principal host for several species. In fact, Amblyomma as a group utilizes a wide range of hosts, which is different from the situation in other genera of Ixodidae (Guglielmone et al. Reference Guglielmone, Robbins, Apanaskevich, Petney, Estrada-Peña and Horak2014). Our new taxon in Burmese amber confirms the presence (see also Grimaldi et al. Reference Grimaldi, Engel and Nascimbene2002) of Amblyomma in the Cretaceous of Southeast Asia. It is only the third tick species to be described from this deposit and the first to be formally placed in an extant genus. Amblyomma can thus be traced back approximately 99 million years. Together with an opilioacarid mite from the same amber deposit (Dunlop and de Bernardi, Reference Dunlop and de Bernardi2014), these Cretaceous ticks also represent the oldest records of parasitiform acarids in general.

Phylogeny and divergence times

With respect to the phylogenetic position of Amblyomma, there is a basic division of hard ticks into the Prostriata group, restricted to the genus Ixodes, and the Metastriata group containing all the other genera (e.g. Black and Piesman, Reference Black and Piesman1994). In Prostriata the anal groove extends anterior to the anus, while in Metastriata the anal groove is located posterior to the anus (Beati and Keirans, Reference Beati and Keirans2001; Nicholson et al. Reference Nicholson, Sonenshine, Lane, Uilenberg, Mullen and Durden2009). We should note that for the genus Ixodes most authors now recognize a split between the Australian and non-Australian species, or have even questioned the monophyly of the genus (e.g. Klompen et al. Reference Klompen, Black, Keirans and Norris2000). In overview, Barker and Murrell (Reference Barker and Murrell2004, Fig. 1) proposed a working hypothesis for hard ticks of the form [Ixodes (Bothriocroton (Amblyomma (Haemaphysalis + Rhipicephalinae and Hyalommine genera)))]. This reflects the older, non-cladistic, scheme of Hoogstraal and Aeschlimann (Reference Hoogstraal and Aeschlimann1982) and the same basic pattern was also recovered in the molecular phylogeny of Mans et al. (Reference Mans, de Klerk, Pienaar, Castro and Latif2012, Fig. 2) using 18S rDNA; although other genes gave slightly different results (see their Fig. 3) such as the non-monophyly of Amblyomma.

Fig. 3.

Phylogenetic tree largely based on Mans et al. (Reference Mans, de Klerk, Pienaar, Castro and Latif2012) with the fossil record of the main genera superimposed. Circles indicate the known fossil occurrences with their estimated dates in millions of years. The inferred origination dates of the major clades are based on Mans et al. although we should caution that all of them had error bars of about ±20 million years. Colour scheme: green (Nuttalliellidae), blue (Argasidae), purple (Ixodidae: Prostriata), red (Ixodidae: Metastriata). Poinar's extinct genera are assumed to be metastriates too, possibly close to Amblyomma (see text for details).

There are numerous proposals, summarized by de la Fuente (Reference de la Fuente2003, Fig. 8), for when ticks – or specifically hard ticks – are thought to have originated. Most were derived, in part, from the fossil record of their typical modern host species. For example, Hoogstraal (Reference Hoogstraal1985) inferred late Palaeozoic or early Mesozoic origins for argasid-like ticks in general, with amblyommid ticks present on reptile hosts as early as the Permian and hyalommine and rhipicephaline tick lineages evolving later on mammalian hosts in the Cretaceous and Cenozoic, respectively. In fact, published inferences on tick origins range from as old as the Devonian (Oliver, Reference Oliver1989; Dobson and Barker, Reference Dobson and Barker1999), with amphibians as putative hosts, to as young as the Cretaceous (Black and Piesman, Reference Black and Piesman1994; Nava et al. Reference Nava, Guglielmone and Mangold2009): a difference of almost 300 million years! Klompen et al. (Reference Klompen, Black, Keirans and Oliver1996) also criticized the assumption that tick phylogeny is determined by the phylogeny of their hosts; i.e. that the early derivative ticks must be those that live on reptiles today. Mans et al. (Reference Mans, de Klerk, Pienaar, Castro and Latif2012: Table 2) estimated divergence times directly using molecular clock methods. Their results include origins for the entire Ixodida in the late Carboniferous (319 ± 23 Ma), the family Ixodidae around the Permian–Triassic boundary (249 ± 23 Ma), and the Metastriata radiating in the Early Cretaceous (124 ± 17 Ma). Thus the Late Cretaceous Burmese amber records of Amblyomma are not much younger than Mans et al.’s estimated divergence time for metastriate ticks in general. Fossils also constrain the split between Amblyomma and its putative sister-group (i.e. Haemaphysalis + rhipicephalines + hyalommines) to at least 99 Ma.

The extinct Burmese amber genera have not been formally integrated into the phylogeny of living taxa. The position of the anal groove is unhelpful here as both C. burmanicum and C. vetulum were described without an anal groove (Poinar and Brown, Reference Poinar and Brown2003; Poinar and Buckley, Reference Poinar and Buckley2008); or at least none could be resolved in the material available. A better guide is the presence of marginal festoons in these Cretaceous fossils. These structures are absent in the prostriate Ixodes and strongly suggest that the two extinct Burmese genera are also metastriate ticks such as Amblyomma. We should also mention de la Fuente's (Reference de la Fuente2003) observation that C. burmanicum resembles Aponomma (= either Bothriocroton or Amblyomma) and comments in Mans et al. (Reference Mans, de Klerk, Pienaar, Castro and Latif2012) that these extinct species are probably close to Amblyomma. Transposing the (albeit limited) fossil record of the ticks onto the current phylogenetic hypothesis (Fig. 3, see also Mans et al. Fig. 4) yields a framework evolutionary scenario. Nuttalliellidae lacks a fossil record. Argasidae is known since the Cretaceous but is estimated to have split from Ixodidae in the Permian. Ixodes is known from the Eocene but is predicted to have split from the metastriate lineage in the early Triassic. The modern metastriate genera are inferred to have radiated in the Cretaceous.

Corrections to the tick fossil record

Origins of the most recently diverged hard tick genera – namely Haemaphysalis, Dermacentor, Hyalomma, Rhipicephalus and Boophilus – were previously constrained to an Eocene divergence date of at least 49 Ma by de la Fuente's (Reference de la Fuente2003: Fig. 6) report of a Hyalomma sp. from Baltic amber. However, during the preparation of the present manuscript, it was pointed out to us (Ekaterina Sidorchuk, personal communication) that de la Fuente's amber fossil is not a tick. In fact, it is a rake-legged mite (Acariformes: Caeculidae), a fact clearly indicated by the large inward-facing spines on the forelegs which are very typical for this group of predatory mites and not seen in Hyalomma or any other tick genus. de la Fuente's (Reference de la Fuente2003) paper contains a further misidentification (Ekaterina Sidorchuk, personal communication). The soft ticks figured from Miocene Dominican amber (Fig. 7) are large parasitengonids. It may also be necessary to further check the identity of the larval Ixodes from Baltic amber (de la Fuente, Reference de la Fuente2003: Fig. 1) and larval ticks from Miocene Dominican amber (his Fig. 4), but this is difficult from the photographs and would require restudy of the original material. Removal of the amber Hyalomma record means that the oldest fossil constraint for the five derived metastriate tick genera listed above is the subfossil D. reticulatus mentioned by Kulczyński in Schille (Reference Schille1916) from the ear of an extinct rhinoceros. Its ca. 1 Ma age is clearly much too young for realistically dating when the genus evolved and means that we must currently rely on molecular clock methods to estimate cladogenesis dates for Haemaphysalis, Dermacentor, Hyalomma, Rhipicephalus and Boophilus.

Palaeobiogeography

A last point of interest is the fact that Southeast Asia has a complex geological history (e.g. Heine and Müller, Reference Heine and Müller2005; Metcalfe, Reference Metcalfe, Hall, Cottam and Wilson2011, Reference Metcalfe2013; Seton et al. Reference Seton, Müller, Zahirovic, Gaina, Torsvik, Shephard, Talsma, Gurnis, Turner, Maus and Chandler2012). The region containing modern Myanmar was originally interpreted as having been part of the so-called Sibumasu terrane, which is thought to have rifted from the northern (i.e. Australian) part of Gondwana in the late Palaeozoic/early Mesozoic and collided with the Indochina plate by the Late Cretaceous. This led to a hypothesis that Burmese amber arthropods could have arrived in Asia by rafting across the Sibumasu terrane from Australia; see e.g. Dunlop and de Bernardi (Reference Dunlop and de Bernardi2014) for a scenario along these lines involving an opilioacarid mite. A challenge to this hypothesis is the fact that back when the Sibumasu terrane is thought to have rifted from Gondwana (creating the Meso-Tethys Ocean), the landmass may actually have been covered by shallow seas. Also, much of Australia at this time was thought to have been covered in ice, and Sibumasu was still linked to Gondwana via the Lhasa block, Argoland and South West Borneo blocks (see e.g. Metcalfe, Reference Metcalfe, Hall, Cottam and Wilson2011). If this model is correct, the survival of terrestrial arthropods on the Sibumasu terrane after separation from Australia seems unlikely.

More recently, the area containing the source of Burmese amber has been interpreted as having been on the West Burma terrane instead; see Broly et al. (Reference Broly, Maillet and Ross2015: Fig. 1) for a map of how the various elements may have accreted together to form modern Myanmar. As discussed for a Burmese amber spider by Selden et al. (Reference Selden, Zhang and Ren2016), one hypothesis is that the West Burma terrane rifted from northern Australia in the Late Jurassic at ca. 156 Ma, and collided with the Sibumasu terrain the Late Cretaceous at about 80 Ma. In this scenario, at the time of amber deposition (ca. 99 Ma) the fauna would have been on an island which had been separated from Australia for about 75 million years. However, Metcalfe (Reference Metcalfe2013) provided evidence for a much earlier (Devonian) separation from Australia and an earlier (Jurassic) collision of the West Burma terrane with Eurasia. In this model the Burmese amber fauna could potentially have arrived from Eurasia at some time between the Jurassic and the mid-Cretaceous.

With respect to ticks, Klompen et al. (Reference Klompen, Black, Keirans and Oliver1996) argued that basal taxa among both prostriate and metastriate ticks predominantly come from Australia today, which could imply that at least the Ixodidae have their origins here. Given that modern Amblyomma are strongly associated with a Gondwanan distribution (see above) it would be instructive to compare estimated dates of cladogenesis with some of these dates for major events in palaeobiogeography (see also Mans et al. Reference Mans, de Klerk, Pienaar, Castro and Latif2012: Fig. 4). Caution is needed in dating ancient geographical splits between continents, and complete physical separation of landmasses may postdate the start of a split by a considerable period of time. Upchurch (Reference Upchurch2008) reviewed several competing models for Gondwana – albeit with a focus on fossil vertebrates – and recognized four potential scenarios. In the Samafrica model, West Gondwana (South America + Africa) separated from East Gondwana (Antarctica, Australia and Indo-Madagascar) during the mid-Jurassic (perhaps ca. 180 Ma). This seems to be the most widely accepted scenario; see also Gibbons et al. (Reference Gibbons, Whittaker and Müller2013) for example. In the Africa-first model, Africa separated from the rest of Gondwana during the Cretaceous while South America was still in contact with East Gondwana until the Late Cretaceous. In the multistage scenario elements of the previous hypotheses are combined, and in the Pan-Gondwana hypothesis the southern continents were still connected, at least at their southern tips, until the Late Cretaceous; perhaps as late as 80 Ma.

If the Samafrica model is correct, current molecular estimates for the Cretaceous radiation of the metastriate ticks (Fig. 3) postdate the Jurassic dissolution of Gondwana into an eastern and western province. Genera such as Amblyomma may show a Gondwanan distribution today, but current estimates of their origination dates correspond to a time in which Gondwana may have already separated into what would become the modern continents. In this hypothesis, either the molecular dates are too young, or modern patterns of biogeography have to be explained by alternative mechanisms. Furthermore, we still have to explain the presence of Amblyomma in the Cretaceous of Southeast-Asia. If its origins are Gondwanan, then the northern route was potentially closed by the breakup of Pangaea and the separation of Gondwana from Laurasia as early as ca. 220 Ma. If its ancestors rafted from Australia on the West Burma terrane, then in Metcalfe's (Reference Metcalfe2013) model the rafting lineage must have separated from the Australian tick fauna around 360–420 million years ago. This seems highly unlikely as it would require these animals to have radiated into modern genera back in the Devonian, which significantly predates the Late Carboniferous molecular estimates (see above) of tick origins.

A final possibility is that Amblyomma actually originated in Eurasia – again perhaps during the Cretaceous as part of this metastriate radiation – and arrived (and was fossilized) in the West Burma region via a northern route long after it had collided with Asia. As noted above, Upchurch's (Reference Upchurch2008) scenarios for the dissolution of Gondwana are largely based on fossil vertebrate data. However, there are numerous examples of plants and animals distributed both in former Gondwanan regions and (often as fossils) in the northern hemisphere. Examples include palpimanoid spiders (Wood et al. Reference Wood, Matzke, Gillespie and Griswold2013, and references therein), ants (Zryanin, Reference Zryanin2015), hemipterans (Szwedo et al. Reference Szwedo, Stroiński and Lin2015), neuropterans (Wedmann and Makarkin, Reference Wedmann and Makarkin2007) and branchiopod crustaceans (Korovchinsky, Reference Korovchinsky2006; Van Damme and Sinev, Reference Van Damme and Sinev2013). The implication here is that these groups were once globally distributed across both the northern and southern continents, but at some stage (perhaps in response to glaciation) either became extinct in the north and/or migrated south. This has been referred to as the ousted relicts (Eskov and Golovatch, Reference Eskov and Golovatch1986) or ejected relicts (Korovchinsky, Reference Korovchinsky2006) hypothesis. Such a scenario should also be borne in mind when considering how Amblyomma came to be so widespread in the former Gondwana region today: did it really originate here, or is it a relict of a once much wider distribution? A final thought is that several species of Amblyomma parasitize birds today, in which case trans-oceanic dispersal through flight remains a possibility.