Phylogeography of Begonia luzhaiensis suggests both natural and anthropogenic causes for the marked population genetic structure

Han-Yau Huang,Hsun-An Yang,Yan Liu,Yu-Hsin Tseng,Wei-Bin Xu,Ching-I Peng,Kuo-Fang Chung

doi:10.1186/s40529-019-0267-9

Abstract

BackgroundSino-Vietnamese limestone karsts (SVLK) are a biodiversity hotspot rich in endemic plant species associated with caves and cave-like microhabitats. Based on phylogenetic studies of Begonia sect. Coelocentrum, a species-rich and characteristic SVLK clade, geographic isolation caused by extensive and continuous karstification was proposed as the major driving force triggering population diversification and geographic speciation. To test this proposition, population genetics and phylogeography of Begonia luzhaiensis were investigated using EST-SSR markers and the chloroplast trnC-ycf6 intergenic spacer.ResultsF statistics, Bayesian clustering analysis, AMOVA, and PCoA of both data sets all indicated substantial population differentiation and significant isolation by distance. Nested clade phylogeographic analyses inferred that historical fragmentations have been prominent, congruent with Guangxi’s geohistory of karstification as well as suggesting a mountain chain in northeastern Guangxi could have also acted as a major geographic barrier. A Bayesian skyline plot (BSP) indicated a slight decline in effective population size at 75,000 years ago (75 Kya), coinciding with the last glacial period during which the increased aridity in East Asia had retarded karstification, negatively affecting the populations of B. luzhaiensis. However, BSP detected a continuous and further population decline until the present time even though summer monsoons have resumed since the end of the last glacial maximum.ConclusionsThe microevolution patterns of B. luzhaiensis support that limited gene flow would have greatly enhanced the effects of random genetic drift and has been a major factor promoting diversification in Begonia, highly congruent with previous proposition. Based our study, we further propose that the arrival of Paleolithic Homo sapiens whose activities centered around limestone caves could have had further impacts on the populations of B. luzhaiensis, resulting in additional population decline. Further habitat destruction could have resulted from the transition from hunter gathering to food-producing societies ca. 20–10 Kya and the development of agriculture ca. 10 Kya in South China. Implications of the current study for SVLK plant conservation are also discussed.

Highlights

Sino-Vietnamese limestone karsts (SVLK) are a biodiversity hotspot rich in endemic plant species associated with caves and cave-like microhabitats
Given the highly fragmented nature of the cave and cave-like microhabitats (Fig. 1c) across the Sino-Vietnamese limestone karsts inhabited by B. luzhaiensis, our results demonstrate that geographic isolation could have played a pivotal role in generating the strong population differentiation of the Clade Sino-Vietnamese limestone Begonia (SVLB) as proposed by Chung et al (2014)
The microevolution patterns of B. luzhaiensis indicate that genetic drift enhanced by limited gene flow could have been the major factor promoting population diversification in Begonia, strongly suggesting the importance of extensive karstification in shaping the species diversity of the Sino-Vietnamese limestone karsts

Summary

Introduction

Sino-Vietnamese limestone karsts (SVLK) are a biodiversity hotspot rich in endemic plant species associated with caves and cave-like microhabitats. The limestone flora of Guangxi is especially noted for a suite of plant genera with exceedingly highly levels of endemism and restricted distribution almost exclusively confined to the ‘twilight zone’ (Poulson and White 1969) of caves and cave-like microhabitats (Fig. 1c) (Xu et al 2012; Chung et al 2014; Monro et al 2018) These narrowly distributed limestone plants—e.g., Aspidistra Ker Gawl., Begonia L., the fern genus Polysticum Roth, Impatiens L., and gesneriad genus Primulina Hance, etc.— present intriguing study systems for investigating plant speciation (Chung et al 2014). The major driving forces that created this plant diversity and the great richness of these narrow-endemic plants in caves of limestone karsts in South China remain poorly understood

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