Research Article: Tick–Host–Pathogen Interactions: Conflict and Cooperation

Date Published: April 21, 2016

Publisher: Public Library of Science

Author(s): José de la Fuente, Margarita Villar, Alejandro Cabezas-Cruz, Agustín Estrada-Peña, Nieves Ayllón, Pilar Alberdi, Virginia L. Miller.


Partial Text

Ticks are blood-feeding arthropod ectoparasites that transmit pathogens that constitute a growing burden for human and animal health worldwide [1–3]. Only second to mosquitoes as vector of human diseases and the first vector of animal diseases, ticks transmit bacterial, parasitic, and viral pathogens [1]. One of these pathogens is the intracellular bacterium Anaplasma phagocytophilum, which is vectored primarily by Ixodes tick species and is the causative agent of human granulocytic anaplasmosis (HGA), equine and canine granulocytic anaplasmosis, and tick-borne fever of ruminants [1]. This pathogen is a good model because recent analysis of the molecular interactions between Ixodes tick vectors, A. phagocytophilum, and host cells showed pathogenic effects of both ticks and pathogens but also revealed the mutual beneficial effects of the tick–host–pathogen molecular interactions [4–7].

It has been established that ticks produce a feeding lesion and inhibit host hemostatic, immune, and inflammatory responses to complete feeding, while pathogens manipulate host and tick biological processes to facilitate infection, multiplication, and transmission [4–7]. At the same time, both ticks and hosts react to tick infestation and/or pathogen infection by activating different mechanisms to fight against tick infestations and limit pathogen infection [4–7]. Therefore, the generally accepted view is that tick infestation and pathogen infection produce detrimental effects on both hosts and ticks that highlight a conflict between hosts, ticks, and pathogens (Fig 1A; see also S1 Video) [5,7]. The evolutionary processes show that coevolution includes interactions between organisms that can produce both conflict and cooperation [8], but the latter has been largely ignored for tick–host–pathogen interactions. However, the conflict between ticks, hosts, and pathogens also reveals cooperation between them benefiting ticks and pathogens and to a lesser extent hosts, leading to mutual beneficial effects of the tick–host–pathogen molecular interactions (Fig 1B; see also S1 Video). The conflict and cooperation in tick–host–pathogen interactions are analyzed in detail in the following sections with examples summarized in Table 1.

The evolution of the tick–host–pathogen molecular interactions resulted in conflict and cooperation between them, with mutual beneficial effects for ticks, hosts, and pathogens (see S1 Video). These results illustrate coevolutionary mechanisms by which pathogens manipulate tick protective responses to facilitate infection while preserving tick feeding and vector capacity to guarantee survival of both pathogens and ticks (Fig 2). The conflict between hosts, ticks, and pathogens has been well characterized. However, the beneficial effects are being discovered for ticks and pathogens and require additional research to provide more evidence for their presence in vertebrate hosts. As discussed here for ticks and A. phagocytophilum, these coevolutionary mechanisms probably apply to other arthropod vectors and transmitted pathogens.




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