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.

Fig 1. The network of interactions between tick genera and life stages (L, larvae; N, nymphs; A, adults) and the families of hosts.

Only the genera and stages of ticks are labeled to improve readabilty. S2 Fig includes the same figure with all the nodes labeled. Nodes are sequentially colored to represent clusters, with nodes of the same color belonging to the same cluster. The size of each node is porportional to its betweenness centrality (BNC), and the size of the label is proportional to its weighted degree (WD). The width of the links is proportional to the weighted number of interactions recorded between hosts and ticks.

Fig 2. The betweenness centrality (BNC, converted to natural log of value + 1) of Aves and Reptilia hosts (alphabetically, at left) for each group of tick genera and life stages (bottom).

A, adults; L, larvae; N, nymphs.

Fig 3. The BNC (converted to natural log of value + 1) of the families of Rodentia, Insectivora, Carnivora, and Artiodactyla hosts (alphabetically, at left) for each group of tick genera and life stages (bottom).

A, adults; L, larvae; N, nymphs.

Fig 4. The loss of connectivity in the networks of larvae, nymphs, and adults of the tick genus Amblyomma and the genus Hyalomma.

Loss of connectivity is calculated after removing hosts randomly (Random, yellow), or after removing hosts in decreasing order of their BNC (red) or of their WD (blue).

Fig 5. The loss of connectivity in the networks of larvae, nymphs, and adults of the genus Ixodes and the genus Rhipicephalus.

Loss of connectivity is calculated after removing hosts randomly (Random, yellow), or after removing hosts in decreasing order of their BNC (red) or of their WD (blue).