Rapid responses of soil microorganisms improve plant fitness in novel environments

Abstract

Global change is challenging plant and animal populations with novel environmental conditions, including increased atmospheric CO(2) concentrations, warmer temperatures, and altered precipitation regimes. In some cases, contemporary or "rapid" evolution can ameliorate the effects of global change. However, the direction and magnitude of evolutionary responses may be contingent upon interactions with other community members that also are experiencing novel environmental conditions. Here, we examine plant adaptation to drought stress in a multigeneration experiment that manipulated aboveground-belowground feedbacks between plants and soil microbial communities. Although drought stress reduced plant growth and accelerated plant phenologies, surprisingly, plant evolutionary responses to drought were relatively weak. In contrast, plant fitness in both drought and nondrought environments was linked strongly to the rapid responses of soil microbial community structure to moisture manipulations. Specifically, plants were most fit when their contemporary environmental conditions (wet vs. dry soil) matched the historical environmental conditions (wet vs. dry soil) of their associated microbial community. Together, our findings suggest that, when faced with environmental change, plants may not be limited to "adapt or migrate" strategies; instead, they also may benefit from association with interacting species, especially diverse soil microbial communities, that respond rapidly to environmental change.

Fig. 1.

Effects of microbe history (dry- or wet-adapted) and contemporary soil moisture (dry or wet soil) on plant fruit number (A), flower number (B), and flowering date (C). Error bars indicate back-transformed least squares means ± 1 SEM.

Fig. 2.

Multivariate ordination showing the effects of microbe history, plant history, and contemporary soil moisture on microbial community composition. Microbe history affected the composition of soil fungi (Upper) and bacteria (Lower), as indicated by the strong separation of samples along PCoA axis 1. Dashed ellipses contain dry-adapted microbial assemblages, and solid ellipses include wet-adapted microbial assemblages. PERMANOVA confirmed the effect of the microbe-history treatment on both fungal and bacterial composition (P = 0.001). Although not as strong as microbe history, contemporary soil moisture (white symbols, dry; gray symbols, wet) significantly affected the composition of bacteria (P = 0.039) and marginally affected the composition of fungi (P = 0.096). In contrast, plant history (dry plants, circles; wet plants, squares) had no effect on fungal or bacterial composition (P = 0.55 and P = 0.22, respectively). Ordinations were created with the output of PCoA, and the percent variation explained by each PCoA axis is presented in parentheses in each axis label.

Fig. 3.

Microbe history and contemporary soil moisture (dry, white bars; wet, gray bars) altered plant-available soil N (NH₄⁺ and NO₃⁻). Plant-available N was higher in dry contemporary soil-moisture treatments than in wet contemporary soil-moisture treatments, especially for soils containing a wet-adapted microbial community (microbe history × contemporary moisture, F_1,8 = 29.04, P = 0.0007). Error bars indicate least squares means ± 1 SEM.