An inbreeding perspective on the effectiveness of wildlife population defragmentation measures – a case study on wild boar (Sus scrofa) of Veluwe, The Netherlands

Abstract

Pervasive inbreeding is a major genetic threat of population fragmentation and can undermine the efficacy of population connectivity measures. Nevertheless, few studies have evaluated whether wildlife crossings can alleviate the frequency and length of genomic autozygous segments. Here, we provided a genomic inbreeding perspective on the potential effectiveness of mammal population defragmentation measures. We applied a SNP-genotyping case study on the ~2500 wild boar Sus scrofa population of Veluwe, The Netherlands, a 1000-km2 Natura 2000 protected area with many fences and roads but also, increasingly, fence openings and wildlife crossings. We combined a 20K genotyping assessment of genetic status and migration rate with a simulation that examined the potential for alleviation of isolation and inbreeding. We found that Veluwe wild boar subpopulations are significantly differentiated (FST-values of 0.02-0.13) and have low levels of gene flow. One noteworthy exception was the Central and Southeastern subpopulation, which were nearly panmictic and appeared to be effectively connected through a highway wildlife overpass. Estimated effective population sizes were at least 85 for the meta-population and ranged from 31 to 52 for the subpopulations. All subpopulations, including the two connected subpopulations, experienced substantial inbreeding, as evidenced through the occurrence of many long homozygous segments. Simulation output indicated that whereas one or few migrants per generation could undo genetic differentiation and boost effective population sizes rapidly, genomic inbreeding was only marginally reduced. The implication is that ostensibly successful connectivity restoration projects may fail to alleviate genomic inbreeding of fragmented mammal populations. We put forward that defragmentation projects should allow for (i) monitoring of levels of differentiation, migration and genomic inbreeding, (ii) anticipation of the inbreeding status of the meta-population, and, if inbreeding levels are high and/or haplotypes have become fixed, (iii) consideration of enhancing migration and gene flow among meta-populations, possibly through translocation.