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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 plantOenothera 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.
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Dormancy in the origin, evolution and persistence of life on Earth
Life has existed on Earth for most of the planet’s history, yet major gaps and unresolved questions remain about how it first arose and persisted. Early Earth posed numerous challenges for life, including harsh and fluctuating environments. Today, many organisms cope with such conditions by entering a reversible state of reduced metabolic activity, a phenomenon known as dormancy. This process protects inactive individuals and minimizes the risk of extinction by preserving information that stabilizes life-system dynamics. Here, we develop a framework for understanding dormancy on early Earth, beginning with a primer on dormancy theory and its core criteria. We hypothesize that dormancy-like mechanisms acting on chemical precursors in a prebiotic world may have facilitated the origin of life. Drawing on evidence from phylogenetic reconstructions and the fossil record, we demonstrate that dormancy is prevalent across the tree of life and throughout deep time. These observations lead us to consider how dormancy might have shaped nascent living systems by buffering stochastic processes in small populations, protecting against large-scale planetary disturbances, aiding dispersal in patchy landscapes and facilitating adaptive radiations. Given that dormancy is a fundamental and easily evolved property on Earth, it is also likely to be a feature of life elsewhere in the universe.
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- PAR ID:
- 10569565
- Publisher / Repository:
- Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 292
- Issue:
- 2038
- ISSN:
- 1471-2954
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2024.2035
