Evolution repeats itself in replicate long-term studies in the wild

Abstract The extent to which evolution is repeatable is central to understanding the role of determinism and chance in the history of life, with implications for basic and applied science 1–5 . Real-time studies of evolutionary dynamics in replicated laboratory populations have revealed repeatable evolution by natural selection, but also a role for chance mutation 6–11 . In contrast to the laboratory, replicated, long-term studies of real-time evolution in the wild are rare. Such studies are required to help establish general principles of evolution and to compliment those based on the fossil record 5 , but are challenging to implement because time cannot simply be sped up with more effort. Here we demonstrate repeatable evolutionary changes in the frequency of cryptic color-pattern morphs of a stick-insect, using three decades of field data and 10 replicate studies that each study span at least a decade. We find predictable ‘up-and-down’ fluctuations in stripe frequency in all populations and demonstrate experimentally that these involve negative frequency-dependent selection (NFDS). Adding complexity, these fluctuations rely on demographic and selective variability that pushes populations away from equilibrium, such that they reliably move back towards it via NFDS. Finally, we show with genomic analyses that contingency in which mutations arise also affects crypsis at larger temporal and phylogenetic scales. Thus, evolution from existing variation is repeatable, but mutation adds complexity even for traits evolving deterministically under natural selection. The findings highlight how evolution can be better understood by the joint effects of selection and mutation than by either process in isolation.