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

Abstract

Habitat loss contributes to extinction risk in multiple ways. Genetically, small populations can face an "extinction vortex" -- a positive feedback loop between declining fitness and declining population size. Two distinct genetic mechanisms can drive a long-term extinction vortex: i) ineffective selection in small populations allows deleterious mutations to fix, driving "mutational meltdown", and ii) smaller populations generate fewer beneficial mutations essential for long-term adaptation, a mechanism we term "mutational drought". To determine their relative importance, we ask whether, for a population near its critical size for persistence, changes in population size have a larger effect on the beneficial vs. deleterious component of fitness flux. In stable environments, we find that mutational drought is nearly as significant as mutational meltdown. Drought is more important than meltdown when populations must also adapt to a changing environment, unless the beneficial mutation rate is extremely high. Linkage disequilibria from background selection under realistically high deleterious mutation rates modestly increase the importance of mutational drought. Long-term conservation efforts should consider adaptive potential, not just deleterious load.