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).