A Pleistocene legacy structures variation in modern seagrass ecosystems

Abstract

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.

Keywords: biogeography; climate; foundation species; genetic structure.

FIG. 1.

Variation in eelgrass growth form and genetic structure across the Northern Hemisphere. (A) Map of the 50 ZEN sites, with symbol color corresponding to ocean (Pacific, green; Atlantic, blue) and light green showing geographic distribution of eelgrass. (B) Variation in eelgrass growth form and biomass by site (SI Appendix, Fig. S1 and Table S1 for site names). Numbers list mean canopy height (H), shoot density (D), and belowground biomass (B) for eelgrass populations at the extremes of the distributions. (C) Variation among sites in neutral genetic markers of evolutionary history, indexed by genetic axes FCA1 and FCA2 summarizing variation across 24 microsatellite loci. Eelgrass growth form and biomass represent the first two axes from a PCA of six eelgrass growth and morphological characteristics (SI Appendix, Table S9). (C, Inset) A neighbor-joining tree of pairwise F_ST distances among all populations, with the size of the symbol proportional to the inverse value of PC_z1; larger symbols denote longer, more forest-like canopies. In both B and C the percentage of variation explained by each axis is shown.

FIG. 2.

Genetic predictors of eelgrass growth form and biomass across Atlantic (blue) (A and B) and Pacific (green) sites (C and D). Plots of partial effects of genetic structure (FCA2) on eelgrass growth form (PC_z1) and biomass (PC_z2) show residual variation attributable to genetic FCA2 after controlling for all other influences (denoted by | Z) in the best model chosen by AICc (SI Appendix, Tables S6 and S7). Values of PC_z2 are inverted such that biomass rises along the y axis. Regression lines and 95% CIs are shown for those predictors with P < 0.05.

FIG. 3.

Effects of eelgrass form and environmental predictors on periphyton (A, B, E, F) and invertebrate biomass (C, D, G, H) across Atlantic (blue) and Pacific (green) sites. Plots show partial effects of eelgrass form (PC_z1) and biomass (PC_z2) on periphyton and invertebrate biomass per bottom (core) area (g dry mass core⁻¹) after controlling for all other influences (denoted by | Z) in the best model chosen by AICc (SI Appendix, Tables S6 and S7). Conventions are as in Fig. 2. See SI Appendix, Tables S2 and S4–S6 for full model results.

FIG. 4.

Influences of environment and evolutionary history on variation in growth form (A, B) and biomass (C, D) of eelgrass and associated organisms (E-H) across the north Atlantic and Pacific oceans. Bars show direct and indirect effects of environmental drivers and eelgrass genetic composition (history) as a weighted sum of the effect sizes (standardized partial regression coefficients) contributed by abiotic environment (PC_e1, PC_e2, PC_e3) and evolutionary history (FCA1, FCA2); see Methods for calculations. Coefficients are from the best model chosen by AICc for each (log₁₀) response variable (SI Appendix, Tables S6 and S7).