Phylogeography of Quercus variabilis based on chloroplast DNA sequence in East Asia: multiple glacial refugia and Mainland-migrated island populations

Abstract

The biogeographical relationships between far-separated populations, in particular, those in the mainland and islands, remain unclear for widespread species in eastern Asia where the current distribution of plants was greatly influenced by the Quaternary climate. Deciduous Oriental oak (Quercus variabilis) is one of the most widely distributed species in eastern Asia. In this study, leaf material of 528 Q. variabilis trees from 50 populations across the whole distribution (Mainland China, Korea Peninsular as well as Japan, Zhoushan and Taiwan Islands) was collected, and three cpDNA intergenic spacer fragments were sequenced using universal primers. A total of 26 haplotypes were detected, and it showed a weak phylogeographical structure in eastern Asia populations at species level, however, in the central-eastern region of Mainland China, the populations had more haplotypes than those in other regions, with a significant phylogeographical structure (N(ST= )0.751> G(ST= )0.690, P<0.05). Q. variabilis displayed high interpopulation and low intrapopulation genetic diversity across the distribution range. Both unimodal mismatch distribution and significant negative Fu's F(S) indicated a demographic expansion of Q. variabilis populations in East Asia. A fossil calibrated phylogenetic tree showed a rapid speciation during Pleistocene, with a population augment occurred in Middle Pleistocene. Both diversity patterns and ecological niche modelling indicated there could be multiple glacial refugia and possible bottleneck or founder effects occurred in the southern Japan. We dated major spatial expansion of Q. variabilis population in eastern Asia to the last glacial cycle(s), a period with sea-level fluctuations and land bridges in East China Sea as possible dispersal corridors. This study showed that geographical heterogeneity combined with climate and sea-level changes have shaped the genetic structure of this wide-ranging tree species in East Asia.

Figure 1. Distribution of 50 Q. variabilis populations (codes in Table 1) and 26 cpDNA haplotypes.

The insert in the right bottom corner shows an overview of study area. The light gray shadow area is the current natural distribution of Q. variabilis , .

Figure 2. BEAST-derived chronograms of 26 haplotypes of Q. variabilis.

The numbers above the branches are posterior probabilities (PP>0.6). Node ages are labeled in the nodes selectively based on posterior probabilities.

Figure 3. The phylogenetic network of 26 cpDNA haplotypes of Q. variabilis.

Circle size is proportional to the frequency of a haplotype over all the populations, with the largest circle representing the most abundant haplotype. Each line between haplotypes represents a mutational step; the number noted between two parallel bars indicates the number of hypothetical missing haplotypes. The small solid white circles represent existing un-sampled haplotypes or extinct ancestral haplotypes.

Figure 4. Bayesian skyline plot.

The x axis is time of mutations per site before present, and the y axis is the expressed population size estimated in units of N_eµ (N_e: effective population size, µ: mutation rate per haplotype per generation), Dark line represents median inferred Neµ, blue lines mark the 95% highest probability density (HPD) intervals.

Figure 5. Ecological niche modelling.

Predicted distribution probability (in logistic value) is shown in each 2.5 arc-min pixel, based on the palaeodistribution modelling at present (0BP) (a) and at the last glacial maximum (LGM) (21KaBP) (b). The distribution of river systems on the exposed East China Sea during the LGM was drawn from Shota et al. (2012). Occurrence records of Q. variabilis at present are also plotted as black points in the maps.