How do genetic relatedness and spatial proximity shape African swine fever infections in wild boar?

Abstract

The importance of social and spatial structuring of wildlife populations for disease spread, though widely recognized, is still poorly understood in many host-pathogen systems. In particular, system specific kin relationships among hosts can create contact heterogeneities and differential disease transmission rates. Here, we investigate how distance-dependent infection risk is influenced by genetic relatedness in a novel wild boar ( Sus scrofa) - African swine fever (ASF) system. We hypothesized that the infection risk would correlate positively with proximity and relatedness to ASF-infected individuals but expected those relationships to weaken with distance between individuals due to decay in contact rates and genetic similarity. ASF infection risk was shaped by the number of infected animals throughout the zone of potential contact (0-10 km) but not beyond it. This effect was the strongest at close distances (0-2 km) and weakened further on (2-10 km), consistent with decreasing probability of contact. Overall, there was a positive association between genetic relatedness to infectees and infection risk within the contact zone but this effect varied in space. In the high-contact zone (0-2 km), infection risk was not influenced by relatedness when controlled for the number of ASF-positive animals. However, infections were more frequent among close relatives indicating that familial relationships could have played a role in ASF transmission. In the medium-contact zone (2-5 km), infection risk and frequency of paired infections were associated with relatedness. Relatedness did not predict infection risk in low- and no-contact zones (5-10 and >10 km, respectively). Together, our results indicate that the number of nearby infected individuals overrides the effect of relatedness in shaping ASF transmission rates which nevertheless can be higher among close relatives. Highly localized transmission highlights the possibility to control the disease if containment measures are employed quickly and efficiently.