Host preferences support the prominent role of Hyalomma ticks in the ecology of Crimean-Congo hemorrhagic fever

Abstract

Crimean-Congo hemorrhagic fever virus (CCHFV) is a tick-borne zoonotic agent that is maintained in nature in an enzootic vertebrate-tick-vertebrate cycle. Hyalomma genus ticks have been implicated as the main CCHFV vector and are key in maintaining silent endemic foci. However, what contributes to their central role in CCHFV ecology is unclear. To assess the significance of host preferences of ticks in CCHFV ecology, we performed comparative analyses of hosts exploited by 133 species of ticks; these species represent 5 genera with reported geographical distribution over the range of CCHFV. We found that the composition of vertebrate hosts on which Hyalomma spp. feed is different than for other tick genera. Immatures of the genus Hyalomma feed preferentially on species of the orders Rodentia, Lagomorpha, and the class Aves, while adults concentrate mainly on the family Bovidae. With the exception of Aves, these hosts include the majority of the vertebrates consistently reported to be viremic upon CCHFV infection. While other tick genera also feed on these hosts, Hyalomma spp. almost completely concentrate their populations on them. Hyalomma spp. feed on less phylogenetically diverse hosts than any other tick genus, implying that this network of hosts has a low resilience. Indeed, removing the most prominent hosts quickly collapsed the network of parasitic interactions. These results support the intermittent activity of CCHFV foci: likely, populations of infected Hyalomma spp. ticks exceed the threshold of contact with humans only when these critical hosts reach adequate population density, accounting for the sporadic occurence of clinical tick-transmitted cases. Our data describe the association of vertebrate host preferences with the role of Hyalomma spp. ticks in maintaining endemic CCHFV foci, and highlight the importance of host-tick dynamics in pathogen ecology.

Author summary

Crimean-Congo hemorrhagic fever virus (CCHFV), a cause of severe hemorragic disease in humans, is maintained in nature in a tick-vertebrate-tick enzootic cycle characterized by silent persistence of endemic foci with intermittent epidemics. Most studies support ticks of the genus Hyalomma as the main CCHFV vectors, but some laboratory reports and field studies also allude to other tick species that may be responsible for virus circulation. Here we converted the tick-host interactions of 133 species of ticks with reported geographical distribution over the range of CCHFV into a network of relationships. By a series of network analyses, we found that immatures of the genus Hyalomma are unique in their hosts preferences among the examined tick genera. Immatures of the genus Hyalomma concentrate on rodent and rabbit hosts, which most efficiently support CCHFV maintenance and transmission by ticks in nature. Based on these data, we formulate the hypothesis that the ecological relationships between Hyalomma spp. and their hosts form a delicate equilibrum that differentiates human epidemics from periods of silent CCHFV maintenance.