Population genetics of the nidicolous soft tick Ornithodoros phacochoerus in the context of African swine fever sylvatic cycle

Abstract

Ticks of the species Ornithodoros phacochoerus are endophilic soft ticks which infest warthog burrows. Like other Ornithodoros of the O. moubata species complex, O. phacochoerus is a vector of the African swine fever virus and participates in the maintenance of the virus among warthogs in the sylvatic cycle in Southern and Eastern African countries. In this study, the population genetic structure of O. phacochoerus was investigated using sixteen microsatellite markers. After sampling campaigns that took place between 2020 and 2022, we analyzed 684 ticks from 21 warthog burrows and resting sites from Coutada 9 Game Reserve, Macossa District, Mozambique, and 138 ticks from 3 warthog burrows and resting sites from Gorongosa National Park, Gorongosa District, Mozambique. Burrows and resting sites are regularly used by the common warthog Phacochoerus africanus which is thought to be responsible for the movements of O. phacochoerus between sites. After genotyping, the observed genetic variation followed a model of isolation by distance with a structure at the level of the sampling sites (burrows and resting sites). Gorongosa National Park and Coutada 9 Game Reserve appeared to be completely isolated from each other in terms of gene flow, and Coutada 9 Game Reserve showed a clear signature of a bottleneck effect. Effective population sizes within sampling sites were quite low (4.1 individuals), with an estimated migration rate of 35% and a mean dispersal distance of 209 meters per tick generation. These results suggested frequent tick movements between burrows at a small geographic scale, due to warthog movements between the burrows. As both wildlife conservation areas are positive for African swine fever virus, these results reinforce the suspected role of the ticks in the sylvatic cycle of the virus, as infected ticks could be moved from one burrow to another, maintaining the presence of the virus in several sites of the conservation areas. This confirms the importance of maintaining buffer zones around conservation areas, buffer zones that should remain free of any domestic pigs to prevent vector spillover from the sylvatic cycle to the domestic cycle.