Evolution and seed dormancy shape plant genotypic structure through a successional cycle

Abstract

Significance Studies that experimentally examine evolution have provided critical insight in biology. Indeed, rigorous and replicated laboratory experiments have revealed parallel evolution and have proved essential to understanding evolutionary processes. Nonetheless, a typical limitation of such work is the lack of ecological realism. We report on a decade-long field experiment with a native plant (common evening primrose) that advances our understanding of how populations adapt to environmental change. In particular, we address whether the common strategy of seed dormancy significantly alters the evolutionary trajectory of populations. We find that population genetic diversity is restored following a period of sustained dormancy. Nonetheless, the impact of past natural selection persisted under some conditions. Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plant Oenothera biennis, which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change.