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Currents are unique drivers of oceanic phylogeography and thus determine the distribution of marine coastal species, along with past glaciations and sea-level changes. Here we reconstruct the worldwide colonization history of eelgrass (Zostera marinaL.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Two west-to-east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival ofZ. marinain the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present there for ~243 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. 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.

 

The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well‐established systems. Here, we examine genomic signals of selection in the eelgrassZostera marinaacross temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay there is very little overlap in signals of selection at the SNP level, despite most polymorphisms being shared across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.

 

One objective of eco‐evolutionary dynamics is to understand how the interplay between ecology and evolution on contemporary timescales contributes to the maintenance of biodiversity. Disturbance is an ecological process that can alter species diversity through both ecological and evolutionary effects on colonization and extinction dynamics. While analogous mechanisms likely operate among genotypes within a population, empirical evidence demonstrating the relationship between disturbance and genotypic diversity remains limited. We experimentally tested how disturbance altered the colonization (gain) and extinction (loss) of genets within a population of the marine angiospermZostera marina(eelgrass). In a 2‐year field experiment conducted in northern California, we mimicked grazing disturbance by migratory geese by clipping leaves at varying frequencies during the winter months. Surprisingly, we found the greatest rates of new colonization in the absence of disturbance and that clipping had negligible effects on extinction. We hypothesize that genet extinction was not driven by selective mortality from clipping or from any stochastic loss resulting from the reduced shoot densities in clipped plots. We also hypothesize that increased flowering effort and facilitation within and among clones drove the increased colonization of new genets in the undisturbed treatment. This balance between colonization and extinction resulted in a negative relationship between clipping frequency and net changes in genotypic richness. We interpret our results in light of prior work showing that genotypic diversity increased resistance to grazing disturbance. We suggest that both directions of a feedback between disturbance and diversity occur in this system with consequences for the maintenance of eelgrass genotypic diversity.

 

Environmental change is multidimensional, with local anthropogenic stressors and global climate change interacting to differentially impact populations throughout a species’ geographic range. Within species, the spatial distribution of phenotypic variation and its causes (i.e., local adaptation or plasticity) will determine species’ adaptive capacity to respond to a changing environment. However, comparatively less is known about the spatial scale of adaptive differentiation among populations and how patterns of local adaptation might drive vulnerability to global change stressors. To test whether fine‐scale (2–12 km) mosaics of environmental stress can cause adaptive differentiation in a marine foundation species, eelgrass (Zostera marina), we conducted a three‐way reciprocal transplant experiment spanning the length of Tomales Bay, CA. Our results revealed strong home‐site advantage in growth and survival for all three populations. In subsequent common garden experiments and feeding assays, we showed that countergradients in temperature, light availability, and grazing pressure from an introduced herbivore contribute to differential performance among populations consistent with local adaptation. Our findings highlight how local‐scale mosaics in environmental stressors can increase phenotypic variation among neighboring populations, potentially increasing species resilience to future global change. More specifically, we identified a range‐center eelgrass population that is pre‐adapted to extremely warm temperatures similar to those experienced by low‐latitude range‐edge populations of eelgrass, demonstrating how reservoirs of heat‐tolerant phenotypes may already exist throughout a species range. Future work on predicting species resilience to global change should incorporate potential buffering effects of local‐scale population differentiation and promote a phenotypic management approach to species conservation.

 

Mortality and shifts in species distributions are among the most obvious consequences of extreme climatic events. However, the sublethal effects of an extreme event can have persistent impacts throughout an individual’s lifetime and into future generations via within‐generation and transgenerational phenotypic plasticity. These changes can either confer resilience or increase susceptibility to subsequent stressful events, with impacts on population, community, and potentially ecosystem processes. Here, we show how a simulated extreme warming event causes persistent changes in the morphology and growth of a foundation species (eelgrass,Zostera marina) across multiple clonal generations and multiple years. The effect of previous parental exposure to warming increased aboveground biomass, shoot length, and aboveground–belowground biomass ratios while also greatly decreasing leaf growth rates. Long‐term increases in aboveground–belowground biomass ratios could indicate an adaptive clonal transgenerational response to warmer climates that reduces the burden of increased respiration in belowground biomass. These transgenerational responses were likely decoupled from clonal parent provisioning as rhizome size of clonal offspring was standardized at planting and rhizome starch reserves were not impacted by warming treatments. Future investigations into potential epigenetic mechanisms underpinning such clonal transgenerational plasticity will be necessary to understand the resilience of asexual foundation species to repeated extreme climatic events.

 

Multiple disturbances can have mixed effects on biodiversity. Whether the interaction of sequential disturbances drives local extinctions or promotes diversity depends on the severity of biomass reductions relative to any stabilizing and/or equalizing effects generated by the disturbance regimes.

Through a manipulative mesocosm experiment, we examined how warming events in the fall and simulated grazing disturbance (i.e. clipping) in the winter affected the density, biomass and genotypic diversity of assemblages of the clonal seagrassZostera marina.

We show that the interaction of the two disturbance types reduced density and biomass to a greater degree than warming or clipping alone.

The genotype with the highest biomass in the assemblage shifted under the different experimental regimes such that the traits of winners were distinct in the different treatments. The favouring of different traits by different disturbances led to reduced evenness when a single disturbance was applied, and enhanced evenness under multiple disturbances.

We conclude that sequential disturbances can alter the outcome of inter‐genotypic interactions and maintain genotypic diversity in clonal populations. Our study expands the context in which disturbance can influence intraspecific diversity by showing that fluctuating selection may result from the sequential application of different disturbance types and not simply seasonal changes in a single agent.

A freePlain Language Summarycan be found within the Supporting Information of this article.

 

Molecular clocks are the basis for dating the divergence between lineages over macroevolutionary timescales (~10⁵to 10⁸years). However, classical DNA-based clocks tick too slowly to inform us about the recent past. Here, we demonstrate that stochastic DNA methylation changes at a subset of cytosines in plant genomes display a clocklike behavior. This “epimutation clock” is orders of magnitude faster than DNA-based clocks and enables phylogenetic explorations on a scale of years to centuries. We show experimentally that epimutation clocks recapitulate known topologies and branching times of intraspecies phylogenetic trees in the self-fertilizing plantArabidopsis thalianaand the clonal seagrassZostera marina, which represent two major modes of plant reproduction. This discovery will open new possibilities for high-resolution temporal studies of plant biodiversity.

 

Distribution of Earth’s biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate–trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth’s environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass ( Zostera marina ), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems. 

The extent of parallel genomic responses to similar selective pressures depends on a complex array of environmental, demographic, and evolutionary forces. Laboratory experiments with replicated selective pressures yield mixed outcomes under controlled conditions and our understanding of genomic parallelism in the wild is limited to a few well-established systems. Here, we examine genomic signals of selection in the eelgrass Zostera marina across temperature gradients in adjacent embayments. Although we find many genomic regions with signals of selection within each bay, there is little overlap at the SNP level across bays. We do find overlap at the gene level, potentially suggesting multiple mutational pathways to the same phenotype. Using polygenic models we find that some sets of candidate SNPs are able to predict temperature across both bays, suggesting that small but parallel shifts in allele frequencies may be missed by independent genome scans. Together, these results highlight the continuous rather than binary nature of parallel evolution in polygenic traits and the complexity of evolutionary predictability.