Genetically- and environmentally-dependent processes drive interspecific and intraspecific divergence in the Chinese relict endemic genus Dipteronia

Abstract

China is a hotspot of relict plant species that were once widespread throughout the Northern Hemisphere. Recent research has demonstrated that the occurrence of long-term stable refugia in the mountainous regions of central and south-western China allowed their persistence through the late Neogene climate fluctuations. One of these relict lineages is Dipteronia, an oligotypic tree genus with a fossil record extending to the Paleocene. Here, we investigated the genetic variability, demographic dynamics and diversification patterns of the two currently recognized Dipteronia species (D ipteronia sinensis and D . dyeriana). Molecular data were obtained from 45 populations of Dipteronia by genotyping three cpDNA regions, two single copy nuclear genes and 15 simple sequence repeat loci. The genetic study was combined with niche comparison analyses on the environmental space, ecological niche modeling, and landscape connectivity analysis. We found that the two Dipteronia species have highly diverged both in genetic and ecological terms. Despite the incipient speciation processes that can be observed in D. sinensis, the occurrence of long-term stable refugia and, particularly, a dispersal corridor along Daba Shan-west Qinling, likely ensured its genetic and ecological integrity to date. Our study will not only help us to understand how populations of Dipteronia species responded to the tectonic and climatic changes of the Cenozoic, but also provide insight into how Arcto-Tertiary relict plants in East Asia survived, evolved, and diversified.

Keywords: Climatic niche divergence; Dipteronia; Dispersal corridor; Genetic structure; Interspecific/intraspecific divergence.

Graphical abstract

Fig. 1

(A) Geographic distribution of STRUCTURE clusters (K = 3) for Dipteronia, and potential dispersal corridors for D. sinensis at present represented in the background. The color-coded grouping is based to UPGMA clusters (B) UPGMA clustering representation based on the climatic values for the first three axes of the standard principal component analysis (PCA). Population codes are identified in Table S1 (C) Histogram of the STRUCTURE (K = 3, K = 2) assignment test for 45 populations of Dipteronia based on EST-SSRs (D) PCA performed with climatic values for the populations of D. sinensis and D. dyeriana. (E) PCA-env representing global climatic space constructed over all background areas and realized niches of Dipteronia (left, total occurrences dataset, N = 267: DS, 250, DD, 17; right, partial dataset, N = 55: DSE, 23; DSW, 15; DD, 17), plotting a solid line representing 20% of the occurrence density (up), and (F) 100% of occurrence density with a thin line and 100% of available climatic background with a thick line (down). The upper graph includes the contribution and direction of each variable to the two-first components of the PCA-env.

Fig. 2

BEAST-derived chronogram for 17 haplotypes of Dipteronia based on three cpDNA fragments. Blue bars indicate 95% highest posterior densities (HPDs) credibility intervals for node ages (Ma). Posterior probabilities (>0.9) are labelled above nodes. Geological period abbreviations: Pli, Pliocene; Q, Quaternary. Red stars represent calibration points.

Fig. 3

Potential distribution of two Dipteronia species at present, during the Pleistocene (ca. 0.787 Ma; LIG, ca. 130 ka and LGM, ca. 21ka) and during the mid-Pliocene (MIS M2, ca. 3.3 Ma and mPWP, ca. 3.205 Ma), respectively.

Fig. 4

The mean probability of habitat suitability values for three genetic lineages of Dipteronia (DSE, DSW, and DD; N = 45: DSE, 24; DSW, 16; DD, 5) at present, during the Pleistocene (MIS19, ca. 0.787 Ma; LIG, ca. 130 ka, and LGM, ca. 21 ka) and during the mid-Pliocene (MIS M2, ca. 3.3 Ma, and mPWP, ca. 3.205 Ma), respectively.

Fig. 5

cpDNA dispersal corridor of Dipteronia sinensis at present, during the Pleistocene (ca. 0.787 Ma; LIG, ca. 130 ka and LGM, ca. 21ka) and during the mid-Pliocene (MIS M2, ca. 3.3 Ma and mPWP, ca. 3.205 Ma), respectively.