Evolutionary history of a widespread tree species Acer mono in East Asia

Abstract

East Asia has the most diverse temperate flora in the world primarily due to the lack of Pleistocene glaciation and the geographic heterogeneity. Although increasing phylogeography studies in this region provided more proofs in this issue, discrepancies and uncertainty still exist, especially in northern temperate deciduous broad-leaved and coniferous mixed forest region (II). And a widespread plant species could reduce the complexity to infer the relationship between diversity and physiographical pattern. Hence, we studied the evolution history of a widespread temperate tree, Acer mono, populations in region II and the influence of physiographic patterns on intraspecific genetic diversity. Analyses of chloroplast sequences and nuclear microsatellites indicated high levels of genetic diversity. The diversity distribution was spatially heterogeneous and a latitudinal cline existed in both markers. The spatial distribution pattern between genetic diversity within A. mono and the diversity at species level was generally consistent. Western subtropical evergreen broad-leaved forest subregion (IVb) had a unique ancient chloroplast clade (CP3) and a nuclear gene pool (GP5) with dominance indicating the critical role of this area in species diversification. Genetic data and ecological niche model results both suggested that populations in region II disappeared during the last glacial maximum (LGM) and recovered from south of Changbai Mt. and the Korean Peninsula. Two distribution centers were likely during the LGM, one in the north edge of warm temperate deciduous broad-leaved forest region (III) and another in the south edge of region III. This was reflected by the genetic pattern with two spatially independent genetic groups. This study highlights the key role of region III in sustaining genetic diversity in the northern range and connecting diversity between southern and northern range. We elucidated the diversity relationship between vegetation regions which could facilitate the understanding of biodiversity origin and maintenance in East Asia.

Keywords: Acer mono; community assemblage; phylogeography; temperate mixed forests.

Figure 1

(A) Flowers of Acer mono. (B) Samara of A. mono. (C) An A. mono tree in warm temperate deciduous broad-leaved forest.

Figure 2

(A) Geographic distribution of the 33 chloroplast haplotypes. The size of the pies corresponds to sample size of each population. The area in Taihang and Lvliang Mts.(in the black frame) is magnified at the top left. The distribution range of Acer mono represents by the black dash line was modified as Hsu (1992).The different vegetation regions were separated by gray borders and different shadow colors in the map. The brown dash line divided vegetation region IV (subtropical evergreen broad-leaved forest region) into two subregions. The borders of vegetation region and subregion were both drawn according to Zhang (2007). Vegetation region/subregion names were abbreviated as follows: II, temperate coniferous broad-leaved mixed forest region (gray shadow); III, warm temperate deciduous broad-leaved forest region (yellow shadow); IVa, eastern subtropical evergreen broad-leaved forest region (red shadow); IVb, western subtropical evergreen broad-leaved forest region (red shadow). (B) The median-joining network of 33 cpDNA haplotypes. The size of pies is proportional to the haplotype frequency. Solid lines represent mutational steps interconnecting two haplotypes. Each line represents 1 step, except for the lines with additional annotation. The three clades were indicated by surrounding gray dotted line according to consensus tree in Fig. 4.

Figure 3

Phylogenetic trees based on cpDNA haplotypes of Acer mono and other species in Genus Acer. (A) Tree for psbA-trnH; (B) tree for trnF-trnL; (C) tree for rpl16. Values in boxes are the coalescence times of the 3 A. mono cpDNA haplotypes and their 95% confidence intervals. Values on the branches are the posterior probabilities of the branches. Detailed information on all of the haplotypes is provided in Table S4.

Figure 4

Rooted consensus trees for the chloroplast haplotypes. The values on the branches are bootstrap support values for the maximum-likelihood (left) and maximum-parsimony (middle) analyses and the posterior probability (right) of the Bayesian analysis. The sequences of haplotypes with “*”were used in construction of the phylogenetic trees in Fig. 3.

Figure 5

Geographic distribution of gene pools (K = 2). The size of the pies corresponds to sample size of each population. The area in which the Taihang and Lvliang Mts. are found is magnified at the top left. The different vegetation regions were separated by gray borders and different shadow colors in the map. The brown dash line divided vegetation region IV (subtropical evergreen broad-leaved forest region) into two subregions. The borders of vegetation region and subregion were both drawn according to Zhang (2007). Vegetation region/subregion names were abbreviated as followed: II, temperate coniferous broad-leaved mixed forest region (gray shadow); III, warm temperate deciduous broad-leaved forest region (yellow shadow); IVa, eastern subtropical evergreen broad-leaved forest region (red shadow); IVb, western subtropical evergreen broad-leaved forest region (red shadow).

Figure 6

(A) Geographic distribution of gene pools (K = 6) and genetic barriers. The size of the pies corresponds to the sample size of each population. Black lines are genetic barriers, with the width representing the bootstrap value of the barrier. The area in which the Taihang and Lvliang Mts. are found is magnified at the top left. The different vegetation regions were separated by gray borders and different shadow colors in the map. The brown dash line divided vegetation region IV (subtropical evergreen broad-leaved forest region) into two subregions. The borders of vegetation region and subregion were both drawn according to Zhang (2007). Vegetation region/subregion names were abbreviated as followed: II, temperate coniferous broad-leaved mixed forest region(gray shadow); III, warm temperate deciduous broad-leaved forest region (yellow shadow); IVa, eastern subtropical evergreen broad-leaved forest region (red shadow); IVb, western subtropical evergreen broad-leaved forest region (red shadow). (B) Neighbor-joining tree for six gene pools.

Figure 7

(A) The current species distribution of Acer mono simulated using a niche model. (B) The species distribution of A. mono simulated during the LGM using a niche model.