Leaf size variations in a dominant desert shrub, Reaumuria soongarica, adapted to heterogeneous environments

Abstract

The climate in arid Central Asia (ACA) has changed rapidly in recent decades, but the ecological consequences of this are far from clear. To predict the impacts of climate change on ecosystem functioning, greater attention should be given to the relationships between leaf functional traits and environmental heterogeneity. As a dominant constructive shrub widely distributed in ACA, Reaumuria soongarica provided us with an ideal model to understand how leaf functional traits of desert ecosystems responded to the heterogeneous environments of ACA. Here, to determine the influences of genetic and ecological factors, we characterized species-wide variations in leaf traits among 30 wild populations of R. soongarica and 16 populations grown in a common garden. We found that the leaf length, width, and leaf length to width ratio (L/W) of the northern lineage were significantly larger than those of other genetic lineages, and principal component analysis based on the in situ environmental factors distinguished the northern lineage from the other lineages studied. With increasing latitude, leaf length, width, and L/W in the wild populations increased significantly. Leaf length and L/W were negatively correlated with altitude, and first increased and then decreased with increasing mean annual temperature (MAT) and mean annual precipitation (MAP). Stepwise regression analyses further indicated that leaf length variation was mainly affected by latitude. However, leaf width was uncorrelated with altitude, MAT, or MAP. The common garden trial showed that leaf width variation among the eastern populations was caused by both local adaptation and phenotypic plasticity. Our findings suggest that R. soongarica preferentially changes leaf length to adjust leaf size to cope with environmental change. We also reveal phenotypic evidence for ecological speciation of R. soongarica. These results will help us better understand and predict the consequences of climate change for desert ecosystem functioning.

Keywords: Reaumuria soongarica; arid Central Asia; common garden; environmental change; leaf size; local adaptation.

FIGURE 1

Geographic locations of the Reaumuria soongarica populations used in this study. The blue triangles represent the original site of populations grown in the common garden. The four main genetic groups of R. soongarica are indicated by different colors. The purple polygon represents the location of the common garden. Precipitation is measured in millimeters

FIGURE 2

Leaves of the populations of Reaumuria soongarica, R. kaschgarica, and R. trigyna. (a) In situ populations, bar = 2 cm. The WCC, HLG, and WXBS populations of R. soongarica belong to different genetic lineages. Every ten stacked leaves come from the same in situ individual. (b) Common garden populations, bar = 2 cm. Twenty leaves were collected from each individual in the common garden. R. k., R. kaschgarica; R. t., R. trigyna

FIGURE 3

Variations in leaf traits among different populations (a) and different genetic lineages (b–d) of in situ Reaumuria soongarica. Each box plot shows the median, 95% confidence interval, and black dots as outliers. Different letters above each box indicate that there are significant differences in leaf traits among populations (lowercase, p < .05) and among lineages (uppercase, p < .01). R. k., R. kaschgarica; R. t., R. trigyna; WL, western lineage; NL, northern lineage; EL, eastern lineage

FIGURE 4

Principal component analysis of the environments of the 46 sampled sites of Reaumuria soongarica based on the altitude and 19 bioclimatic factors. (a) Environmental divergences along principal components 1 and 2. Each genetic group is highlighted by a different geometric figure. Others include TKS and WSTL populations. BJTD‐CG, the original sites of populations grown in the common garden belong to the BJTD group. (b) Ranked importance of variables based on their loading values in PC1 and PC2. The boxes with many diagonal lines represent negative loading values. The climatic factors related to temperature are indicated by filled boxes with gray, and the bioclimatic variables related to precipitation are highlighted by open boxes. Annotations of all bioclimatic factors are shown in Table 2

FIGURE 5

Relationships between leaf traits and geographic factors for the 30 in situ populations of Reaumuria soongarica. Each point is the mean of a trait in one population ± SD. Units: latitude (°N); altitude (m); longitude (°E)

FIGURE 6

Relationships between leaf traits and climatic factors for the 30 in situ populations of Reaumuria soongarica. (c, f, i) The populations with MAP more than 200 mm were removed in these linear regression analyses. The value for each trait in each population is the mean ± SD. Units: MAT (°C); MAP (mm)

FIGURE 7

Relationships between leaf traits and geographic factors for the common garden populations and six in situ populations from the BJTD group of Reaumuria soongarica. (a) Leaf length with latitude (in situ populations, R² = 0.021, p = .786; common garden populations, R² = 0.275, p = .037). (b) Leaf length with altitude (in situ, R² = 0.165, p = .425; common garden, R² = 0.271, p = .039). (c) Leaf length with longitude (in situ, R² = 0.465, p = .136; common garden, R² = 0.131, p = .168). (d) Leaf width with latitude (in situ, R² = 0.579, p = .079; common garden, R² = 0.110, p = .209). (e) Leaf width with altitude (in situ, R² = 0.564, p = .085; common garden, R² = 0.252, p = .047). (f) Leaf width with longitude (in situ, R² = 0.370, p = .200; common garden, R² = 0.343, p = .017). (g) Leaf length to width ratio (L/W) with latitude (in situ, R² = 0.032, p = .736; common garden, R² = 0.371, p = .012). (h) L/W with altitude (in situ, R² = 0.017, p = .805; common garden, R² = 0.503, p = .002). (i) L/W with longitude (in situ, R² = 0.202, p = .371; common garden, R² = 0.446, p = .005). In (a) to (i), open circles and dashed fitted lines represent the garden populations, and filled circles represent the in situ populations from the BJTD group. The value for each trait in each population is the mean ± SD

FIGURE 8

Relationships between leaf traits and climatic factors for the common garden populations and six in situ populations from the BJTD group of Reaumuria soongarica. (a) Leaf length with MAT (in situ populations, R² = 0.266, p = .295; common garden populations, R² = 0.103, p = .226). (b) Leaf length with MAP (in situ, R² = 0.142, p = .461; common garden, R² = 0.327, p = .021). (c) Leaf width with MAT (in situ, R² = 0.052, p = .665; common garden, R² = 0.198, p = .084). (d) Leaf width with MAP (in situ, R² = 0.886, p = .005; common garden, R² = 0.125, p = .180). (e) Leaf length to width ratio (L/W) with MAT (in situ, R² = 0.219, p = .350; common garden, R² = 0.280, p = .036). (f) L/W with MAP (in situ, R² = 0.0001, p = .983; common garden, R² = 0.434, p = .006). In (a) to (f), open circles and dashed fitted lines represent the garden populations; filled circles and solid fitted lines represent the in situ populations from the BJTD group. The value for each trait in each population is the mean ± SD

FIGURE 9

Partial Mantel tests between the phenotypic distance of leaf traits and environmental distance for the common garden populations and six in situ populations from the BJTD group of Reaumuria soongarica. (a) Mantel tests between environmental distance and geographic distance among the common garden populations and among six in situ populations from the BJTD group. (b–d) Partial mantel tests between the environmental distance and phenotypic distance of leaf length, leaf width, and leaf length to width ratio. In each panel, R² and P value were estimated by Mantel test or partial Mantel test. Fitted slopes were estimated by linear regression analyses