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Novel herbarium resurrection experiment investigates rapid adaptation under climate change

For many plants, a changing climate means coping with hotter, drier, and less predictable conditions. In a recent resurrection experiment, a research team used herbaria collections to assess evolution to water deficit over a short time scale in the arid Southwest and found evidence for rapid plant adaption to drought, largely through shifts in resource allocation. 

by Amelia Keyser-Gibson | 11 March 2024 |@uw_climatereadyplants

In terrestrial ecosystems, one of the impacts of climate change is drought conditions becoming more frequent and severe. For sessile organisms like plants, more arid conditions potentially threaten species persistence. Across the plant kingdom, plants exhibit a diversity of coping mechanisms to withstand water deficit, including the capacity to adapt, acclimate, or to some extent, migrate. While acclimation may help plants withstand a changing climate in the short-term, in order to survive the magnitude predicted environmental change, plants will likely be forced to either adapt or migrate. Evolutionary adaptation has historically been thought of occurring over long time scales and many generations, however there is increasing evidence that adaptation can take place over shorter timescales than initially predicted². Given the rapid rate of environmental shifts under anthropogenic climate change, there remains uncertainty about how quickly plants might adapt or how potential adaptation might buffer species’ vulnerability to a changing climate.

In a recent study in the American Journal of Botany, Christie et al. employ a novel resurrection study, utilizing herbarium samples coupled with contemporary sampling to assess plant adaptation to drought. They specifically test adaptation potential in Plantago patagonica Jacq., a species that self-pollinates with cleistogamous flowers, grows in the arid Southwestern United States and has previously shown local adaptation to water availability³. After identifying existing herbaria collections from populations especially prone to water deficit in recent decades, the team collected seeds from five populations sampled between 2003 and 2014 (the “ancestral” seed source). “Post-drought” or descendant genotypes were sampled in 2019 from the same five populations as the ancestral seed sources to compare the capacity for rapid evolution to novel environmental conditions. Following the successful germination of the majority of herbaria seeds, the next generation was put through a series of trials including different watering treatments, and a terminal drought experiment during which morphological, phenological, and fitness traits were measured and recorded.

The research team observed rapid adaptation (5-16 years timespan) between ancestral and descendant populations. Findings largely consisted of shifts in plant biomass allocation which promoted seedling drought survival. Specifically, the research team found that descendants invested less in seeds (fewer and lighter) and reproductive tissue. Additionally, descendants were also found to focus more on root production, likely enabling these populations to better access limiting water resources, but also more in leaf biomass. This last finding is slightly counterintuitive since larger leaf area means more surface area for water loss via transpiration, and smaller leaves are often seen as an adaption to hotter and drier environments. The observed decreases in investment indicate an attempt to conserve resources under more stressful conditions, though functionally investing more in reproduction and less in biomass production could be advantageous for increasing the chance of offspring persisting in more stressful environments, though the authors cite the lack of competition in the native range of P. patagonica as a possible explanation.

Findings also included small increases in time to mortality in the descendant populations. In the terminal drought experiment, descendants survived drought significantly longer (5%) than ancestors, and this impact also resulted in ancestor plants dying earlier in higher numbers than the descendants. The authors also noted that early germinating plants survived longer, but did not mention controlling for germination time, meaning those individuals could have been at an advantage for having longer to establish prior to the implementation of drought treatment.

Based on significant shifts in allocation findings, and the authors’ note that not all measured traits responded in an adaptive way over the tested generations, it would have been interesting to measure additional traits such as physiological response. Measuring stomatal conductance and characterizing morphology, as well as photosynthetic rates could lend insight into the mechanisms behind allocation shifts. Descendants both surviving drought for longer and producing greater leaf biomass could also indicate a selection for vigor over a response to drought. Given that herbaria samples are typically collected for work in systematics, it is possible that the ancestral collections did not capture the genetic diversity existing in population. Future work into resurrection approaches from herbaria samples could benefit from comparing seed quality from seed banks given the difference in storage conditions, as another potential explanation for smaller plant size in the ancestors could be lower seed quality. No mention was made of any species range shifts or contraction between tested generations, which could lend insight into population-level shifts under drought conditions.

This paper not only presented novel techniques for investigating short-term adaptation under changing climate, but provided interesting commentary on determining if phenotypic change can be considered adaptive. The authors leverage the coupling of increased leaf biomass as well as longer survival time in dependents as phenotypes that increase fitness under drought for this species, though this trend has not been observed more broadly across plant taxa. Throughout the article there was a noted lack of use of the term “acclimation”, instead favoring “plastic response”, though plasticity was also used to describe adaptive shifts over time. Further investigation into genetic underpinnings for phenotypic change, and the capacity of epigenetic mechanisms to shift fitness under stressful conditions will continue to offer clarity in this area.

Typically used primarily for taxonomic work, this paper presents the novel use as herbaria in resurrection experiments. Though not without some limitations, such as seed quality and biases resulting from phenotypes surviving storage, for certain samples and by utilizing an assessment of how well population variability is captured (as done by these authors) herbaria samples provide valuable seed sources. This paper presents additional support for the value of utilizing herbaria collections as an invaluable tool for plant science in the face of anthropogenic climate change, joining recent work which advocates for increasing the use of arboreta and botanic gardens^4,5. Together, botanical collections such as these present untapped potential as natural laboratories and safekeepers of genetic diversity. Projects promoting their use can serve as a template for implementing collections into broader ecological research and champion their preservation as invaluable resources (especially salient as this commentary was written on a week when a major university announced the dissolution of their herbarium).

References

1. Cayan, D. R., Das, T., Pierce, D. W., Barnett, T. P., Tyree, M., & Gershunova, A. (2010). Future dryness in the Southwest US and the hydrology of the early 21st century drought. Proceedings of the National Academy of Sciences of the United States of America, 107(50), 21271–21276.
2. Bodbyl Roels, S. A., and J. K. Kelly. 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65 (9): 2541–2552. doi: 10.1111/j.1558-5646.2011.01326.x.
3. Christie, K., Pierson, N. R., Holeski, L. M., & Lowry, D. B. (2023). Resurrected seeds from herbarium specimens reveal rapid evolution of drought resistance in a selfing annual. American Journal of Botany, 110(12): e16265. https://doi.org/10.1002/ajb2.16265
4. Hirons, A. D., Watkins, J. H. R., Baxter, T. J., Miesbauer, J. W., Male-Muñoz, A., Martin, K. W. E., Bassuk, N. L., & Sjöman, H. (2021). Using botanic gardens and arboreta to help identify urban trees for the future. Plants People Planet, 3(2), 182–193.
5. Meineke, E. K., T. J. Davies, B. H. Daru, and C. C. Davis. Biological collections for understanding biodiversity in the Anthropocene. Philosophical Transactions of the Royal Society, B, Biological Sciences 374: 20170386.