Abstract
Anthropogenic mortality of wildlife is typically inferred from measures of the absolute decline in population numbers. However, increasing evidence suggests that indirect demographic effects including changes to the age, sex, and social structure of populations, as well as the behavior of survivors, can profoundly impact population health and viability. Specifically, anthropogenic mortality of wildlife (especially when unsustainable) and fragmentation of the spatial distribution of individuals (home‐ranges) could disrupt natal dispersal mechanisms, with long‐term consequences to genetic structure, by compromising outbreeding behavior and gene flow. We investigate this threat in African leopards (Panthera pardus pardus), a polygynous felid with male‐biased natal dispersal. Using a combination of spatial (home‐range) and genetic (21 polymorphic microsatellites) data from 142 adult leopards, we contrast the structure of two South African populations with markedly different histories of anthropogenically linked mortality. Home‐range overlap, parentage assignment, and spatio‐genetic autocorrelation together show that historical exploitation of leopards in a recovering protected area has disrupted and reduced subadult male dispersal, thereby facilitating opportunistic male natal philopatry, with sons establishing territories closer to their mothers and sisters. The resultant kin‐clustering in males of this historically exploited population is comparable to that of females in a well‐protected reserve and has ultimately led to localized inbreeding. Our findings demonstrate novel evidence directly linking unsustainable anthropogenic mortality to inbreeding through disrupted dispersal in a large, solitary felid and expose the genetic consequences underlying this behavioral change. We therefore emphasize the importance of managing and mitigating the effects of unsustainable exploitation on local populations and increasing habitat fragmentation between contiguous protected areas by promoting in situ recovery and providing corridors of suitable habitat that maintain genetic connectivity.
Highlights
When assessing the effects of anthropogenic mortality on wildlife populations, managers and policymakers typically consider only direct numerical responses of populations to human-mediated mortality
Harvest can facilitate the spatial reorganization of individuals within populations by creating home-range vacancies that can be filled by neighboring or immigrant conspecifics through a “vacuum effect” (Frank, Leclerc, et al, 2017a)
A consequence of this female philopatry is the spatial formation of adult female kin-clusters, a phenomenon evidenced by the strong spatio-genetic autocorrelation in female–female dyads in both Sabi Sand Game Reserve (SSGR) and Phinda-uMkhuze Complex (PMC)
Summary
When assessing the effects of anthropogenic mortality on wildlife populations, managers and policymakers typically consider only direct numerical responses of populations to human-mediated mortality (poaching, retaliatory conflict, and unregulated trophy hunting; Woodroffe & Ginsberg, 1998). Young male leopards are released from local male–male competition and may exhibit “opportunistic natal philopatry” to avoid the substantial costs of dispersal, undertaking shorter dispersal distances and establishing home-ranges nearer their mothers and sisters (Fattebert, Robinson, Balme, Slotow, & Hunter, 2015b). In such a scenario, the socio-spatial structure of males is expected to approximate the kin-clustered spatial structure of females, which, in the absence of active inbreeding avoidance, promotes increased levels of localized inbreeding (Støen, Bellemain, Sæbø, & Swenson, 2005). We discuss our findings in the context of local population fitness and the broader implications of disrupted dispersal on persistence and functional connectivity across leopard metapopulations throughout protected areas
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