Inescapable bottlenecks: Demographic recovery cannot replenish evolutionary potential over conservation timeframes

Toby Gregory Laszlo Kovacs , Simon Ho , Carolyn J. Hogg, Catherine E. Grueber

Maintaining within-species genetic diversity is a central goal of biodiversity conservation, because it determines a species’ capacity to adapt to environmental change. Species that have experienced population bottlenecks are expected to suffer from an increased risk of extinction unless their genetic diversity is able to recover. A recent study proposed that rapid demographic expansion in a bottlenecked koala population is restoring evolutionary potential through the recovery of rare genetic variants. Using simulations and population genetic models, we argue that evolutionary potential takes thousands of generations to recover after demographic recovery, well beyond a realistic conservation timeframe. This is because adaptation is more likely to occur from standing genetic variation than from de novo mutations, and evolutionary potential is more closely tied to genome-wide heterozygosity than to the number of rare variants. Reanalysis of koala genomic data further supports this, highlighting that functional genetic diversity remains reduced across all allele frequency classes and providing no evidence that evolutionary potential has been restored. Bottleneck-induced loss of diversity also leads to reduced mutational load, but this should be interpreted with caution because it is the conversion of heterozygous to homozygous load in bottlenecked populations that drives the expected increase in genetic load, not the overall mutational load. Our study shows that some genomic indicators of recovery can be misleading when interpreted in isolation, and that demographic recovery alone is not a viable path to restoring the evolutionary potential of threatened species.