East‒West genetic differentiation across the Indo-Burma hotspot: evidence from two closely related dioecious figs

Abstract

Background: Understanding biodiversity patterns and their underlying mechanisms is of interest to ecologists, biogeographers and conservationists and is critically important for conservation efforts. The Indo-Burma hotspot features high species diversity and endemism, yet it also faces significant threats and biodiversity losses; however, few studies have explored the genetic structure and underlying mechanisms of Indo-Burmese species. Here, we conducted a comparative phylogeographic analysis of two closely related dioecious Ficus species, F. hispida and F. heterostyla, based on wide and intensive population sampling across Indo-Burma ranges, using chloroplast (psbA-trnH, trnS-trnG) and nuclear microsatellite (nSSR) markers, as well as ecological niche modeling.

Results: The results indicated large numbers of population-specific cpDNA haplotypes and nSSR alleles in the two species. F. hispida showed slightly higher chloroplast diversity but lower nuclear diversity than F. heterostyla. Low-altitude mountainous areas of northern Indo-Burma were revealed to have high genetic diversity and high habitat suitability, suggesting potential climate refugia and conservation priority areas. Strong phylogeographic structure and a marked east‒west differentiation pattern were observed in both species, due to the interactions between biotic and abiotic factors. Interspecific dissimilarities at fine-scale genetic structure and asynchronized historical dynamics of east‒west differentiation between species were also detected, which were attributed to different species-specific traits.

Conclusions: We confirm hypothesized predictions that interactions between biotic and abiotic factors largely determine the patterns of genetic diversity and phylogeographic structure of Indo-Burmese plants. The east‒west genetic differentiation pattern observed in two targeted figs can be generalized to some other Indo-Burmese plants. The results and findings of this work will contribute to the conservation of Indo-Burmese biodiversity and facilitate targeted conservation efforts for different species.

Keywords: East‒West differentiation; Ficus; Indo-Burma; Phylogeography; Pollinating wasp.

Fig. 1

Geographical distribution of the genetic clusters detected by STRUCTURE for F. hispida (a) and F. heterostyla (c) and bar plots of the membership probabilities of F. hispida (b) and F. heterostyla (d) individuals to the different clusters from the STRUCTURE analysis at K = 2. The pie charts represent the assignment values of the admixed clustering analysis in (a) and (c). Solid black lines define the boundaries between populations in (b) and (d). The populations are roughly arranged according to longitude from west to east. Western clusters are colored red, and eastern clusters are colored blue

Fig. 2

Unrooted neighbor-joining trees showing the relationships among 30 F. hispida (a) and 21 F. heterostyla populations (b) based on the chord distance (Dc) of Cavalli-Sforza and Edwards estimated from 14 nSSR loci. Bootstrap values (> 50%) calculated with 1000 replicates are given at the nodes. The trees are colored according to the results of the structure analysis, and the pie charts at the tips represent the assignment values of the admixed clustering analysis

Fig. 3

Two-dimensional scatter diagram based on principal coordinate analysis of genetic variation in the studied F. hispida (a) and F. heterostyla (b) populations. The pie charts represent the assignment values of the admixed clustering analysis

Fig. 4

The regression of paired F_ST/(1-F_ST) vs. geographic distance was significant for nSSR data in both F. hispida (a) and F. heterostyla (b)

Fig. 5

Maps showing the chloroplast DNA haplotype distribution and median-joining network (in the lower right corner) of F. hispida (a) and F. heterostyla (b) populations. In the network diagrams, circle size is proportional to the number of individuals with the haplotype, and the nodes with a small red diamond represent intermediate haplotypes

Fig. 6

Chronogram of the chloroplast haplotypes of F. hispida (a) and F. heterostyla (b) obtained by BEAST analysis of the psbA-trnH + trnS-trnG dataset. The estimated divergence time/Bayesian posterior probabilities (≥ 0.5) are shown beside the nodes. The red- and blue-colored haplotypes indicate that they were located in the western and eastern populations, respectively

Fig. 7

The results of mismatch distribution analysis and Bayesian skyline plots of F. hispida (a, b) and F. heterostyla (c, d) estimated with cpDNA sequences. The thick solid blue line in b and d is the mean estimate, and the area delimited by the light blue broadband represents the highest posterior density 95% confidence intervals for Ne

Fig. 8

Four scenarios for F. hispida and F. heterostyla based on Approximate Bayesian Computation. ‘East’ and ‘West’ represent the eastern and western cluster identified by STRUCTURE, respectively. N₁, N_1a: The effective population size of eastern cluster at present and at t₁, respectively; N_2,N_2a: The effective population size of western cluster at present and at t₂, respectively; N₃: The effective population size of ancestral populations at t₃. The time (t₁, t₂, t₃) parameters were estimated in generations; PP, posterior probabilities of the scenarios obtained by logistic regression

Fig. 9

Potential distributions of F. hispida predicted using MaxEnt based on nine bioclimatic variables representing the LIG (a), LGM (b), MIH (c), present (d) and future (e) climatic conditions. Warmer colors denote areas with a higher probability of presence. Green dots show the extant occurrence record points of F. hispida. Terrestrial ecoregions of the Indo-Burma region are colored in (f). The black needles and red strikes indicate the population samples of F. hispida and F. heterostyla, respectively