Slower environmental change hinders adaptation from standing genetic variation

Abstract

Evolutionary responses to environmental change depend on the time available for adaptation before environmental degradation leads to extinction. Explicit tests of this relationship are limited to microbes where adaptation depends on the order of mutation accumulation, excluding standing genetic variation which is key for most natural species. When adaptation is determined by the amount of heritable genotype-by-environment fitness variance then genetic drift and/or maintenance of similarly fit genotypes may deter adaptation to slower the environmental changes. To address this hypothesis, we perform experimental evolution with self-fertilizing populations of the nematode Caenorhabditis elegans and develop a new inference model that follows pre-existing genotypes to describe natural selection in changing environments. Under an abrupt change, we find that selection rapidly increases the frequency of genotypes with high fitness in the most extreme environment. In contrast, under slower environmental change selection favors those genotypes that are worse at the most extreme environment. We further demonstrate with a second set of evolution experiments that, as a consequence of slower environmental change, population bottlenecks and small population sizes lead to the loss of beneficial genotypes, while maintenance of polymorphism impedes their fixation in large populations. Taken together, these results indicate that standing variation for genotype-by-environment fitness interactions alters the pace and outcome of adaptation under environmental change.