Flying ticks: anciently evolved associations that constitute a risk of infectious disease spread
© de la Fuente et al. 2015
Received: 1 September 2015
Accepted: 8 October 2015
Published: 15 October 2015
Ticks are important vectors of emerging zoonotic diseases affecting human and animal health worldwide. Ticks are often found on wild birds, which have been long recognized as a potential risk factor for dissemination of ticks and tick-borne pathogens (TBP), thus raising societal concerns and prompting research into their biology and ecology. To fully understand the role of birds in disseminating some ticks species and TBP, it is important to consider the evolutionary relationships between birds, ticks and transmitted pathogens. In this paper we reviewed the possible role of birds in the dissemination of TBP as a result of the evolution of host-tick-pathogen associations. Birds are central elements in the ecological networks of ticks, hosts and TBP. The study of host-tick-pathogen associations reveals a prominent role for birds in the dissemination of Borrelia spp. and Anaplasma phagocytophilum, with little contribution to the possible dissemination of other TBP. Birds have played a major role during tick evolution, which explains why they are by far the most important hosts supporting the ecological networks of ticks and several TBP. The immune response of birds to ticks and TBP has been largely overlooked. To implement effective measures for the control of tick-borne diseases, it is necessary to study bird-tick and bird-pathogen molecular interactions including the immune response of birds to tick infestation and pathogen infection.
Birds and risks of dissemination of tick-borne diseases
Vector-borne diseases are a growing problem for human and animal health worldwide . Ticks are important vectors of emerging zoonotic diseases and both adult and immature stages are often found on wild birds . Birds have been long recognized as a potential risk factor for dissemination of ticks and tick-borne diseases, thus raising societal concerns and prompting research into their biology and ecology. Birds can potentially transport tick-borne pathogens (TBP) that cause disease in humans and animals such as A. phagocytophilum (human and animal granulocytic anaplasmosis and tick-borne fever in ruminants), Rickettsia spp. (human and animal rickettsiosis), Borrelia spp. (human and animal borreliosis) by different means including transportation of ticks, infection with TBP and transmission to feeding ticks [3–10]. Therefore, although it has never been demonstrated that ticks or TBP have been established in a new locality after being transported by birds, evidence strongly suggests that this event may be possible .
To address the possible risks for dissemination of tick-borne infectious diseases by birds, it is important to understand the evolution of bird-tick-pathogen interactions and the ecologic and genetic drivers of these associations. Furthermore, understanding how birds respond to tick infestations and pathogen infection may provide new interventions for reducing the risks for spreading of ticks and transmitted pathogens by birds. Recent reviews have addressed some of these questions [2, 8, 11], but in this paper we reviewed the possible role of birds in the dissemination of tick-borne diseases as a result of the evolution of host-tick-pathogen associations.
To review the possible role of birds in the dissemination of tick-borne diseases as a result of the evolution of host-tick-pathogen associations, we focused as a model on bacterial pathogens of the genera Borrelia, Rickettsia, Anaplasma, Ehrlichia and Neoehrlichia. Viruses and protozoan pathogens and Relapsing fever Borrelia spp. were excluded from the analysis because certain tick-bird-pathogen associations such as those for Babesia, Theileria and viruses are difficult to support with current reports from the literature. Additionally, host-tick-pathogen networks were calculated from the compilation of published data spanning the period 1990–2014 by focusing as an example on taxonomic associations among these organisms in the western Palearctic only. The western Palearctic was defined as countries included within the borders marked by Scandinavia in the north, the Azores in the Atlantic, North African countries in the south, and the Ural Mountains and Turkey in the east. Therefore, some of the pathogens such as Relapsing fever Borrelia spp. were excluded from the analysis because they are poorly reported in the target region thus providing limited evidence for tick-host-pathogen association for these species. We explicitly excluded the records on domestic animals and the Anaplasma spp. such as A. marginale and A. ovis that primarily infest domestic animals, because it has been demonstrated that this data distorts the actual ecological structure underlying the “natural” network (see Additional file 1). Pathogen positive ticks and hosts considered in the analysis included both infected and pathogen DNA-positive records in published data.
The Ancient Egyptians and Greeks were aware of ticks. Tick fever is referred to in an Egyptian papyrus dated 1550 BC and in the Odyssey (850 BC) Homer wrote, “there lays Argos, the dog, full of dog flies” (kynoraistes, believed to be ticks) [12, 13]. In Egyptian hieroglyphs, “Sparrow” was used as a determinative for “common” and “small” but also for “bad”  for birds becoming a pest but perhaps also for carrying ectoparasites such as ticks. Since then ticks have been recognized as dangerous for human and animal health.
Fossil ticks are difficult to find but the record supports tick-bird co-evolution . Fossil ticks that have birds as possible hosts range from 90–94 Mya (Cretaceous) to 15–40 Mya (Tertiary) . These species include Carios jerseyi, Ixodes succineus, I. tertiarius, Amblyomma near testudinis, unclassified Ixodes, Hyalomma, Amblyomma species, and Ornithodoros antiquus . Interestingly, the oldest fossil corresponds to C. jersey (90–94 Mya) with the hypothesis that the tick fed on sea-faring birds to explain how it was found in New Jersey amber . Recently, Borrelia-like spirochetes were found in fossil Amblyomma sp. in Dominican amber , providing the first record of spirochete-like cells associated with fossil ticks and providing additional support for the possible role of birds in disseminating this pathogen. Additionally, a tick discovered in prehistoric Arizona coprolite of human origin supports the hypothesis that ticks were a potential source of disease and that ancient people ate ectoparasites .
Evolutionary considerations of bird-tick-pathogen associations
The evolutionary relationships between birds, ticks and transmitted pathogens are important to understand the role of birds in disseminating ticks and TBP. Bird species that support ticks and TBP are older (37.68 ± 19.08 Mya) than Eutherian (mammals) (18.27 ± 15.22 Mya) species (Fig. 2b), suggesting that the evolutionary associations between ticks, pathogens and birds may precede that of ticks, pathogens and mammals.
Despite radiations of non-Australian Ixodida and Metastriata, Neognathae and Palaeognathae birds and mammals (Rodentia, Carnivora and Artiodactyla) concurred approx. 100 Mya, it is interesting to note that the divergence of Rodentia (approx. 91.8 Mya), Carnivora (approx. 84.9 Mya) and Artiodactyla (approx. 87.3 Mya) , which are important components of extant tick-host networks (Fig. 2a), occurred before the radiation of abundant tick genera (5, 6 and 7 in Fig. 3). However, as mentioned before, molecular clock analysis of divergence times for host species showed that mammals (including Rodentia, Carnivora and Artiodactyla) to which ticks and transmitted pathogens are associated with are relatively younger than birds (p < 0.0001) (Fig. 2b). Altogether, these facts suggest that tick-bird associations are provably older than tick-mammal associations.
Regarding TBP, the results suggest that the association between ticks and birds are probably recent when compared to that of ticks and TBP (i.e. family Anaplasmataceae). The common ancestor of Rickettsia was a free-living bacterium that adapted to intracellular endosymbiosis with protists approx. 525–775 Mya [27, 28]. The transition to infecting arthropods occurred approx. 425–525 Mya, around the Cambrian explosion, when most metazoan phyla appeared . Our molecular clock analysis is consistent with this hypothesis about the origin of Rickettsia and placed the divergence of Anaplasma and Ehrlichia approx. 150 Mya (Fig. 3), which is consistent with the divergence of the ancestor of the Rickettsia group (including groups hydra, torix and rhizobius) . Several Rickettsia, mainly of the Spotted Fever Group, are associated to and transmitted by ticks . Interestingly, the radiation of Rickettsia approx. 50 Mya concurred with the radiation of Anaplasma (approx. 61.32 Mya), Ehrlichia (approx. 41.51 Mya) and that of tick genera Amblyomma (approx. 70 Mya), Bothriocroton (approx. 73 Mya), Dermacentor (approx. 60 Mya) and Haemaphysalis (approx. 62 Mya).
Taken together, these results support the hypothesis that bird-tick-pathogen associations evolved in the Cretaceous approx.125 Mya, thus suggesting that ticks adapted to feed on birds, the likely host for early Anaplasma and Ehrlichia species long before mammalian hosts appeared on Earth. Consequently, birds likely played an important role in the dissemination of ticks and TBP to mammals.
Bird-tick-pathogen ecological and phylogenetic associations
In summary, the study of host-tick-pathogen associations revealed a prominent role for birds in the dissemination of Borrelia spp. and A. phagocytophilum, with little contribution to the possible dissemination of other rickettsiae.
Bird response to tick infestations and pathogen infection and possibilities for control of vector-borne diseases
Little information is available on the avian immune response to tick infestations and pathogen infection, which are a fundamental component of host-tick-pathogen interactions . Ectoparasite-specific antibody response and non-specific antibody titers positively correlate with tick infestations in chicken and sand martin, respectively . Furthermore, although selection on birds has favored a variety of possible adaptations for dealing with ectoparasites , genetic traits associated with tick resistance in birds have not been defined . It has been suggested that the prevalence of ticks on different bird species depends mainly on the degree of feeding on the ground . However, Clayton et al.  provide a number of adaptation mechanisms by which birds combat ectoparasite infestations. Recently, Benson et al.  demonstrated links between the predominantly extinct deep time adaptive radiation of non-avian dinosaurs and the phenomenal diversification of birds, via continuing rapid rates of evolution along the phylogenetic stem lineage. Furthermore, recent analyses revealed that pan-avian genomic diversity covaries with adaptations to different lifestyles and convergent evolution of traits . Some of these mechanisms may be related to the adaptation to combat tick infestations and selection of genetic traits for tick resistance.
These results suggest that it is necessary to characterize bird response to tick infestations and pathogen infection using Next Generation Sequence (immunogenomics, transcriptomics, proteomics, and other omics) technologies and bioinformatics to identify genetic markers and mechanisms associated with tick infestations. As shown in other host species, these results together with the characterization of bird response to vaccination with ectoparasite-derived antigens may result in new interventions to control tick infestations and pathogen infection in birds [40–42], thus reducing the risks for spreading ticks and TBP.
Birds are central elements in the ecological networks of ticks, hosts and TBP. To fully understand the role of birds in disseminating some ticks species and TBP, it is important to consider the evolutionary relationships between birds, ticks and transmitted pathogens. The study of host-tick-pathogen associations reveals a prominent role for birds in the dissemination of Borrelia spp. and A. phagocytophilum, with little contribution to the possible dissemination of other TBP. The implementation of effective measures to control tick-borne diseases is associated with the understanding of ecological factors affecting the dynamics of TBP transmission and biological mechanisms such as immune responses resulting from the interaction between ticks, reservoir hosts and pathogens. The immune response of birds to ticks and TBP has been largely overlooked. Birds have played a major role during tick evolution, which explains why they are by far the most important hosts supporting the ecological networks of ticks and several TBP. To implement effective measures for the control of tick-borne diseases, it is necessary to study bird-tick and bird-pathogen molecular interactions including the immune response of birds to tick infestation and pathogen infection.
Part of this research was supported by EU FP7 ANTIGONE project number 278976.ACC was supported by a grant from the Ministère de l’Education Supérieure et de la Recherche of France.
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