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

Abstract

Background: Sino-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. Results: F 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. Conclusions: The 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.