Extinction vortices are driven more by a shortage of beneficial mutations than by deleterious mutation accumulation

Natural populations are increasingly at risk of extinction due to climate change and habitat loss or fragmentation. The long-term viability of small populations can be threatened by an “extinction vortex” — a positive feedback loop between declining fitness and declining population size. Two distinct mechanisms can drive an extinction vortex: i) ineffective selection in small populations allows deleterious mutations to fix, driving “mutational meltdown”, and ii) fewer individuals produce fewer of the novel beneficial mutations essential for long-term adaptation, a mechanism we term “mutational drought”. We measure the relative importance of each mechanism, on the basis of how sensitive beneficial vs. deleterious components of fitness flux are to changes in census population size near the critical population size at which fitness is stable. We derive analytical results given linkage equilibrium, complemented by simulations that capture the complex linkage disequilibria that emerge under high deleterious mutation rates. Even in the absence of environmental change, mutational drought can be nearly as important as mutational meltdown. Real populations must also adapt to a changing environment, making mutational drought more important. A partial exception is that mutational drought is somewhat less important when the beneficial mutation rate is high, although its contribution remains substantial. Linkage between deleterious and beneficial mutations drives the critical population size substantially higher and increase (albeit modestly) the importance of mutational drought.