Fig. 1 schematically represents the relationships between selected Borrelia and tick species. The figure shows the pathogen-vector pairing between B. hermsii and O. hermsi, Borrelia turicatae and Ornithodoros turicata, B. lonestari and Amblyomma americanum, and B. theileri and Boophilus microplus, but the occurrence of more than one species of Borrelia in I. scapularis and I. ricinus. The relationships between expanded groups of Ixodes spp. and LB group species are shown in Fig. 3. The species are presented as branches of the respective phylograms. Less-well characterized tick species have tentative placements, which are based on less-complete sequence data, in the figure. The branches were manually arranged for more convenient presentation but without the aim of a formal or robust demonstration of co-evolution.
The figure demonstrates the overlapping and complex relationships between the Ixodes ticks and the Borrelia spirochaetes. I. ricinus is the vector of at least five different LB group species: B. afzelii, B. garinii, B. burgdorferi and Borrelia valaisiana in Fig. 3, as well as Borrelia lusitaniae (Hubalek & Halouzka, 1997). B. burgdorferi is probably not even of Palaearctic origin (Marti Ras et al., 1997). It was probably imported to Europe from North America during the last two or three centuries, which is comparatively recent by evolutionary standards. B. garinii is transmitted by I. ricinus and I. persulcatus, which are sister taxa in a clade, and also by Ixodes uriae, a tick of sea-birds of the Arctic and Antarctic. I. uriae, along with Ixodes holocyclus and other Australasian region species, comprise a separate clade from other Ixodes spp. (Klompen et al., 2000).
The fairly non-stringent specificity between Ixodes and Borrelia was also demonstrated experimentally. Although some Ixodes species, such as Ixodes cookei and I. holocyclus, were reported as not or poorly competent as vectors of B. burgdorferi (Barker et al., 1993; Piesman & Stone, 1991), others, such as I. hexagonus (Gern et al., 1991), I. pacificus (Lane et al., 1994), Ixodes spinipalpis (Dolan et al., 1997), Ixodes jellisoni (Lane et al., 1999), Ixodes angustus (Peavey et al., 2000), Ixodes muris (Dolan et al., 2000) and Ixodes sinensis (Sun et al., 2003) were able to transmit LB agent species in the laboratory. [Many studies had demonstrated the incompetence of a variety of metastriate ticks to transmit LB agents (Barbour & Fish, 1993).]
In contrast to Ixodes spp. and the LB group of Borrelia spp., there appears to be considerably more specificity between RF group Borrelia spp. and their argasid vectors in terms of vector competence. A summary of the results of several studies of this phenomenon is presented in Fig. 2. Like the transovarial transmission studies, the tick competence studies date from at least 50 years ago and were carried out by different sets of investigators, but because Borrelia-tick associations were the most discriminating means of identifying taxonomically an unknown Borrelia sp., these sorts of studies were frequent at the time and, for the most part, well-controlled and carefully described. (The vector competence studies of Gordon E. Davis and his colleagues at the Rocky Mountain Laboratory of the National Institutes of Health in the 1940s and 1950s provide a particularly rich source of information about the biology of these pathogens and their vectors.)
The figure shows that the only tick that was reported to be able to experimentally transmit a Borrelia sp. other than its usual pair mate was Ornithodoros moubata, the usual vector of B. duttonii in sub-Saharan Africa. This tick was able to transmit to laboratory animals Borrelia crocidurae and Borrelia hispanica as well as B. duttonii. Previously, it had been shown that there was cross-immunity between B. duttonii and B. crocidurae (Schlossberger & Wichmann, 1929). These three species are also highly similar by the criterion of rRNA and other sequences (Marti Ras et al., 1996) and could otherwise be considered as different strains of the same species (A. G. Barbour & J. Bunikis, unpublished findings).
The two other species that O. moubata was reported to have transmitted were B. hermsii and B. parkeri, which are genetically distant from each other and from B. duttonii (Marti Ras et al., 1996) (unpublished studies). However, Davis (1942) also noted that the O. moubata ticks infected with B. hermsii or B. parkeri were smaller than uninfected ticks and demonstrated comparatively low oviposition. Thus infection with the non-concordant species may have lowered the fitness of the ticks. O. moubata also differs from other known Ornithodoros vectors of RF Borrelia spp. in transmitting the infection through coxal fluid as well as or instead of through saliva (Varma, 1956b), and thus may offer a different and less discriminating mode of transmission for spirochaetes.
The genetic trait that restricted the transmission by other ticks appears to be dominant. The F1 generation of mating O. turicata and Ornithodoros parkeri ticks was able to transmit both B. turicatae and B. parkeri (Davis, 1942). Possible natural hybrids of these two species of ticks with the ability to transmit both Borrelia spp. were also observed. This phenomenon also appears to have been observed in the field (Davis & Burgdorfer, 1955). The putative trait may be expressed in the mouthparts or the midgut of the tick. B. duttonii after several passages in mice lost the ability to infect O. moubata feeding on a spirochaetaemic mouse, but ticks were rendered infectious when the same B. duttonii isolate was injected directly into the haemocoel, thereby bypassing the intestine (Varma, 1956a).
While the studies of Davis and others demonstrated a high degree of specificity between a given Borrelia sp. with the species of its vector, Davis did not observe local specificity within species of ticks and Borrelia when ticks and organisms of the same species from different locations in the western US were paired in different combinations in transmission studies (Davis, 1956b).
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