A century-long record of plant evolution reconstructed from a coastal marsh seed bank

Abstract

Evidence is mounting that climate‐driven shifts in environmental conditions can elicit organismal evolution, yet there are sparingly few long‐term records that document the tempo and progression of responses, particularly for plants capable of transforming ecosystems. In this study, we “resurrected” cohorts of a foundational coastal marsh sedge (Schoenoplectus americanus) from a time‐stratified seed bank to reconstruct a century‐long record of heritable variation in response to salinity exposure. Common‐garden experiments revealed that S. americanus exhibits heritable variation in phenotypic traits and biomass‐based measures of salinity tolerance. We found that responses to salinity exposure differed among the revived cohorts, with plants from the early 20th century exhibiting greater salinity tolerance than those from the mid to late 20th century. Fluctuations in salinity tolerance could reflect stochastic variation but a congruent record of genotypic variation points to the alternative possibility that the loss and gain in functionality are driven by selection, with comparisons to historical rainfall and paleosalinity records suggesting that selective pressures vary according to shifting estuarine conditions. Because salinity tolerance in S. americanus is tightly coupled to primary productivity and other vital ecosystem attributes, these findings indicate that organismal evolution merits further consideration as a factor shaping coastal marsh responses to climate change.

Accounting for variability when resurrecting dormant propagules substantiates their use in eco‐evolutionary studies

“…Our findings build on prior work (Blum et al, 2021;Jarrell et al, 2016;Saunders, 2003;Summers et al, 2018), indicating that S. americanus can serve as a model for studying persistent soil-stored seed banks and for using dormant propagules to infer evolutionary change of an ecosystem engineer over ecologically-relevant timescales. Evidence that in situ viability of S. americanus seeds extends for a century or more helps lay the foundation for further inquiry about the ecophysiology, environmental conditions, and evolutionary drivers of aging, decay, and dormancy of soil-stored seeds (Long et al, 2015).…”

“…Our work also offers some guidance for breaking dormancy to assemble depth/age cohorts of S. americanus for time-shift experiments (Blanquart & Gandon, 2013) to explore the role of adaptation in response to past and near-term future environmental change (Bustos-Segura et al, 2014;Davis et al, 2005;Orsini et al, 2013). With further refinement, the use of soil-stored seed banks could provide more realistic contexts, in contrast to space-for-time approaches (Shaw & Etterson, 2012), for inferring the progression of evolution in natural populations (Blum et al, 2021), and thus eventually emerge as a powerful complement to similarly-minded approaches that rely on ex situ seed archives (Etterson et al, 2016;Everingham et al, 2021;Franks et al, 2008;Summers et al, 2018;Weis, 2018).…”

Microbial mediation of salinity stress response varies by plant genotype and provenance over time

“…We conducted a common-garden experiment (Figure 1) using plants derived from seeds comprising an ancestral (c. 100 year-old seeds) and a descendant (c. 10 year-old) age cohort (Summers et al, 2018;Blum et al, 2021; SM and CI exhibit differences in soil biogeochemistry and plant community composition. For instance, SM soils are more organic and have less Fe (Weiss et al, 2004).…”

“…Our findings highlight the potential importance of ecological interactions and evolution in determining the fate of ecosystems experiencing pressures linked to climate change. Natural surveys (Blum et al, 2010) and experiments (Blum et al, 2021;Erickson et al, 2007;Gentile, 2015) have shown that salinity strongly influences the distribution, growth, and phenotype of S. americanus.…”

“…We focused on S. americanus in part because it dominates brackish marshes across the Atlantic and Gulf coasts of North America, where it can govern vital ecosystem processes like carbon cycling and accretion. Prior studies also have demonstrated that S. americanus can be “resurrected” from century‐long soil‐stored seed banks (Summers et al, 2018; Vahsen et al, 2021), and that plants originating from the early 20th century exhibit different heritable responses to salinity and atmospheric carbon dioxide (CO 2 ) relative to descendants (Blum et al, 2021; Gentile, 2015). Building on these findings, we evaluated the potential for microbial mediation of salinity stress by conducting a common‐garden experiment using ancestral and descendant cohorts of S. americanus from two Chesapeake Bay marshes.…”