The evolution of the genetic load during habitat loss and population fragmentation

Abstract Habitat loss and population fragmentation pose severe threats to the survival of many species. Population isolation and the decline in effective population size lead to increased genetic drift and inbreeding. In turn, this reduces neutral diversity, and it also affects the genetic load of deleterious mutations. Here, we analyse the effect of such genomic erosion by designing a spatially explicit model in SLiM to simulate the effects of the recorded habitat loss in Mauritius over the past ~ 250 years. We show that the loss of neutral nucleotide diversity was barely noticeable during the first 100 years of habitat loss, and that it only became apparent when the total amount of suitable habitat had been reduced to circa 25% of the native undisturbed forest. At that time, the census population size had dropped from circa 10,000 individuals to approximately N = 2000 (equivalent to Ne ~ 1000). The decline of neutral diversity continued after the metapopulation had stabilised at low numbers, consistent with the “drift debt” hypothesis. Although a considerable number of deleterious mutations were lost by drift, others increased in frequency. The masked load was thus converted into a realised load, which compromises individual fitness and population viability after much of the native habitat had been lost. Our study shows that historic habitat loss can pose a sustained threat to populations also in future generations, and that the resulting genetic erosion is likely to continue even without further habitat loss. The UN’s Decade on Ecosystem Restoration needs to lead to transformative change to save species from future extinction, and this requires the urgent restoration of natural habitats.