Surfing downhill: when should population range expansion be characterized by reductions in fitness?

Abstract

Deleterious mutations are found in all populations. Their existence at low frequencies is easily understood, but explaining how they reach high frequencies has long been a challenging problem for population geneticists and evolutionary biologists. Some cases of apparently deleterious alleles are explained by pleiotropy or environmental context dependence, but for universally deleterious alleles, two mechanisms are generally invoked to explain how they can reach high frequencies: (i) genetic drift in small populations and (ii) 'hitchhiking' (sensu Maynard Smith J, Haigh J, Genetical Research, 1974, 23, 23-35) involving tight linkage to beneficial mutations. However, these oft-cited explanations do not immediately resolve the problem because many real populations of interest have population sizes and recombination rates that are large enough to render it nearly impossible for all but the most weakly deleterious (i.e. nearly neutral) mutations to establish and persist. Furthermore, both mechanisms are usually silent about patterns of intraspecific variation in mutation load. In this issue, Peischl S, Dupanloup I, Kirkpatrick M, Excoffier L (Molecular Ecology, 2013) develop and explore a mechanism that puts drift and hitchhiking of deleterious mutations into a specific spatial and demographic context: range expansions. Importantly, their findings provide a plausible explanation for puzzling empirical patterns, such as the paradoxical observation that genotypes at the leading edge of a range expansion are sometimes less fit than those in the ancestral range (when fitness is assessed in a common environment).