Discussion
Our results showed that the risk of ASF infection was shaped by interacting effects of spatial proximity and genetic relatedness to infected individuals. Proximity and number of infected animals had consistently positive effect on infection risk throughout the zone of potential contact (0-10 km) but not beyond it, thus fully supporting H1. The number of ASF-positive individuals had the strongest effect on infection risk in the high-contact zone (0-2 km; P1.1), weaker but similar within medium- (2-5 km) and low-contact (5-10km) zones (P1.2), and no effect in the no-contact zone (>10 km; P1.3). There was a positive association between genetic relatedness to infectees and infection risk within the contact zone (0-10 km), supporting H2, but this effect varied in space (H3). In the high-contact zone, infection risk was not influenced by relatedness when controlled for the number of ASF-positive animals. However, infections were more frequent among close relatives, i.e. kin or group members, indicating that familial relationships could have played a significant role in ASF transmission. In the medium-contact zone, infection risk was associated with relatedness and paired infections were more frequent among relatives. For the most part, those results provide support of P3.1. Relatedness did not predict infection risk in low- and no-contact zones (P3.2 and P3.3, respectively).
Social contacts directed towards relatives can lead to increased pathogen transmission within familial groups and local clustering of disease prevalence (Blanchong et al., 2007; Delahay et al., 2000). Social relationships in wild boar tend to be the strongest among closely related group members (Gabor et al., 1999; Podgórski et al., 2018; Podgórski et al., 2014b). Therefore, we predicted a strong effect of relatedness on disease transmission at close distances (0-2-km) due to socially-driven contact heterogeneity. This prediction was not supported in our regression model possibly because at this distance most individuals are highly related and there are not enough unrelated individuals to find statistical significance. However, our descriptive analysis found that individuals which were infected simultaneously (i.e. paired infections) tended to be more related than those uninfected. This trend was particularly noticeable at the upper range of relatedness distribution, i.e. among close kin or group members. Such a pattern is consistent with kin-biased associations in wild boar, particularly among females and young animals, manifested in more regular and longer lasting contacts (Podgórski et al., 2014b; Poteaux et al., 2009) which facilitate disease transmission. Similarly, kinship was shown to drive bovine tuberculosis infections in badger cubs exposed to infectious females in a natal sett (Benton et al., 2016). Inter-group contacts in wild boar occur most frequently at a spatial scale similar to interactions within groups (Podgórski et al., 2018; Yang et al., 2020). This spatial overlap in social connectivity may confound the effects of inter- vs. intra-group transmission. Using relatedness as an indicator of group membership could potentially help untangle those effects. However, in our study the number of ASF-positive individuals in close vicinity was a much stronger predictor of infection risk compared to relatedness. It thus appears that at close distances kin relationships do not have a strong impact on structuring contacts and shaping ASF transmission beyond the closest relatives. Our analysis did not discriminate between infections originating from the contact with infectious carcass and infected live animals. Therefore, it is possible that indirect transmission through infected carcasses and contaminated environment (Chenais et al. 2018) contributed significantly to recorded infections. In fact, indirect transmission accounts for more than half of ASF infections in wild boar population (Pepin et al., 2020). Animals could have come into contact with nearby infected carcass of the individual which was a member of a different but spatially overlapping social group, i.e. was not closely related. Abundance of infectious carcasses in the surrounding environment could thus lead to infection regardless of relatedness and produce confounding effects that masked actual transmission contacts among live animals.
Interestingly, infection risk correlated with relatedness in the medium-contact zone (2-5 km) suggesting that social connectivity with relatives extended beyond the closest group members. This pattern is unlikely to have resulted from the dispersing individuals infected in the natal groups because it typically takes longer to disperse (Podgórski et al., 2014a) than it takes the disease to hamper movements (Blome et al., 2013). To alleviate symptoms of the disease, infected wild boar seek specific habitats which differ from those regularly used (Morelle et al., 2019). Those preferences and restricted mobility of sick animals can separate them from the group and result in dispersion of diseased group members and wide distribution of samples from related individuals. Additionally, kin-directed interactions over larger distances could be maintained by temporal fission-fusion events of core groups, similar to observed in African elephants (Archie et al., 2006) or giraffes (Carter et al., 2013). These dynamics could provide a mechanism for disease transmission among distant relatives. However, fission-fusion dynamics in wild boar has not been systematically studied and it is difficult to tell whether temporal scales of social and disease dynamics would match and help explain patterns observed in our study. Besides relatedness to infected individuals, their number had a strong impact on infection risk within the medium-contact zone which indicates that contacts between groups and/or with infected carcasses played an important role in transmission.
Relatedness did not play a major role in shaping ASF infections beyond 5 km distance. In the low-contact zone (5-10 km), infection risk was influenced only by the number of infected individuals. It is unlikely that direct transmission played a significant role in producing this effect since inter-group contacts are very rare at those distances (Pepin et al., 2016; Podgórski et al., 2018). While a distance of 5-10 km exceeds the size of typical home range, it is within a range of daily travel (Podgorski et al., 2013) and could be covered during dispersal, foraging or mating forays leading to distant transmission events. Those behaviors, however, are not typically seeking contact with kin and particularly in case of mating or dispersal are often seeking non-kin to avoid inbreeding (Archie et al., 2007; Biosa et al., 2015; Hoffman et al., 2007). The observed effect of distant infected individuals on infection risk could be also a by-product of correlated local enzootic dynamics (i.e. spatial and temporal co-occurrence of cases) rather than direct transmission. Spatial clusters of increased ASF prevalence identified previously were measured at 20-40km (Podgórski et al., 2020; Taylor et al., 2021). However, those studies used data aggregated over time periods (months-years) exceeding temporal windows of ASF transmission (days-weeks) and thus could not capture fine-scale disease dynamics well. Our results indicate that ASF outbreaks are even more localized and with realistic transmission times do not exceed 10 km distance. This is supported by strong genetic structuring among infected animals (Fig. S2) and no effect of the number of infected individuals located at >10km on infection risk (Table 2, Fig.3). The spatial limits of transmission highlight the possibility to control outbreaks if containment measures, such as fencing, zoning and carcass removal, are employed immediately and early detection is ensured by effective surveillance.
Together our results show that ASF infection risk declines with distance, matching spatial changes in contact intensity. Infection-causing contacts were structured by relatedness particularly in medium- and, to lesser degree, high-contact zones. At close distances infections were more frequent only among close kin while at medium distances relatedness predicted infections risk more consistently. This indicates that physical kin relationships can extend beyond the immediate social environment and induce differential transmission rates, similarly to transmission of chronic wasting disease in white-tailed deer (Grear et al., 2010). However, infection risk was primarily influenced by the number of infected individuals throughout the high-, medium-, and low-contact zones. This effect was particularly strong at close distances conforming to the previous modeling study which found that most transmission events occur within <1.5 km with some rare events at longer distances (Pepin et al., 2021). Spatially limited transmission is further supported by an insignificant effect of the number of infected individuals present at long distances (> 10 km).