Award: OCE-1829976

Sustaining biodiversity and ecosystems in the long term depends on their adjustment to a rapidly changing climate. Seagrass ecosystems provide important services to people in coastal regions worldwide, fostering vigorous production, habitat for fisheries, processing of nutrient runoff, carbon storage, and erosion control. The worlds most widespread seagrass species, eelgrass (Zostera marina) forms extensive meadows on both sides of the north Atlantic and north Pacific oceans. Variation among individuals in growth, resource use and tolerance of disturbances contribute to an important role for the maintenance of diversity within eelgrass for conservation and restoration, but to date the origin and genetic underpinnings of these important differences are poorly understood, so our predictive power is limited. This project blends seagrass genomics, ecology and physiology to understand global patterns of genetic diversity the impact of that diversity on the functioning of coastal marine ecosystems, and the ability of eelgrass to adapt to a changing climate. First, we reconstruct the worldwide colonization history of eelgrass from its origin in the Northwest Pacific. We find that there have been at least two independent colonizations of the Pacific coast of North America from Japan separated by hundreds of thousands of years. Second, eelgrass arrived in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present in the Atlantic Ocean for about 250 ky (thousand years). Mediterranean populations were founded ~44 kya, while extant distributions along western and eastern Atlantic shores were founded at the end of the Last Glacial Maximum (~19 kya), with at least one major refuge being the North Carolina region, which currently has among the highest local diversity of any Atlantic population studied. The recent colonization and five- to sevenfold lower genomic diversity of the Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans. As Earths environment changes faster than at any time in human history, how this diversity in foundation species will allow organismal traits and ecosystems to adjust to altered conditions is a critical question. By characterizing the structure of the marine plant eelgrass and associated communities at 50 sites across its broad range, we found that eelgrass growth form and biomass retain a legacy of Pleistocene range shifts and genetic bottlenecks that in turn affect the biomass of algae and invertebrates that fuel coastal food webs. The ecosystem-level effects of this ancient evolutionary legacy are comparable to or stronger than effects of current environmental forcing, suggesting that this economically important ecosystem may be unable to keep pace with rapid global change. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems. Our Pacific experiments and genomic surveys demonstrate high genetic diversity and rapid local adaptation to thermal stress along multiple bays and estuaries. First, field experiments show that populations separated by just 2 to 10 km show differences in their tolerance of environmental conditions that match their home sites. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the individual DNA sequence level. We do find overlap at the gene level, suggesting that novel mutations in nearby bays have led to the same ability to tolerate temperature and light stress. Ourresults suggest that eelgrass can rapidly locally adapt to environmental conditions and this needs to be accounted for in restoration activities. Further, separate studies show that plants can acclimate to stress and harden, passing that stress tolerance on to their offspring, perhaps in the form of increased belowground resources to overwinter. Ongoing work tests the relative importance of this plasticity vs adaptation across large geographic gradients of genetic diversity and whether populations in low diversity regions are less adaptable in the face of environmental change. Last Modified: 12/28/2023 Submitted by: JohnJStachowicz