Phylogenetic analyses of Begonia sect. Coelocentrum and allied limestone species of China shed light on the evolution of Sino-Vietnamese karst flora

Abstract

Background: The picturesque limestone karsts across the Sino-Vietnamese border are renowned biodiversity hotspot, distinguished for extremely high endemism of calciphilous plants restricted to caves and cave-like microhabitats that have functioned as biological refugia on the otherwise harsh habitats. To understand evolutionary mechanisms underlying the splendid limestone flora, dated phylogeny is reconstructed for Asian Begonia, a species-rich genus on limestone substrates represented by no less than 60 species in southern China, using DNA sequences of nrITS and chloroplast rpL16 intron. The sampling includes 94 Begonia species encompassing most major Asian clades with a special emphasized on Chinese species.

Results: Except for two tuberous deciduous species and a species with upright stems, a majority of Sino-Vietnamese limestone Begonia (SVLB), including sect. Coelocentrum (19 species sampled) and five species of sect. Diploclinium, Leprosae, and Petermannia, are rhizomatous and grouped in a strongly supported and yet internally poorly resolved clade (Clade SVLB), suggesting a single evolutionary origin of the adaptation to limestone substrates by rhizomatous species, subsequent species radiation, and a strong tendency to retain their ancestral niche. Divergence-time estimates indicate a late Miocene diversification of Clade SVLB, coinciding with the onset of the East Asian monsoon and the period of extensive karstification in the area.

Conclusions: Based on our phylogenetic study, Begonia sect. Coelocentrum is recircumscribed and expanded to include other members of the Clade SVLB (sect. Diploclinium: B. cavaleriei, B. pulvinifera, and B. wangii; sect. Leprosae: B. cylindrica and B. leprosa; sect. Petermannia: B. sinofloribunda). Because species of Clade SVLB have strong niche conservatism to retain in their ancestral habitats in cave-like microhabitats and Begonia are generally poor dispersers prone to diversify allopatrically, we propose that extensive and continuous karstification of the Sino-Vietnamese limestone region facilitated by the onset of East Asian monsoon since the late Miocene has been the major driving force for species accumulation via geographic isolation in Clade SVLB. Morphologically species of Clade SVLB differ mainly in vegetative traits without apparent adaptive value, suggesting that limestone Begonia radiation is better characterized as non-adaptive, an underappreciated speciation mode crucial for rapid species accumulations in organisms of low vagility and strong niche conservatism.

Keywords: Biological refugia; Cave plants; East Asian monsoon; Non-adaptive radiation; Phylogenetic niche conservatism; Sect. Diploclinium; Sect. Leprosae; Sect. Petermannia; Uplift of Tibetan Plateau.

Figure 1

Best-scoring maximum likelihood phylogram. Clade support values (LB: likelihood bootstrap/PB: parsimony bootstrap/PP: posterior probability) larger than 50% are indicated at each node. Dashed branches indicate LB, PB, and PP all smaller than 50%/0.5 while thick branches denote those present in the strict consensus tree of MP analysis and PP ≥0.95. Species in bold denote limestone species distributed in the Sino-Vietnamese limestone karsts (Gu et al.,2007). Arrows point to clades and sections discussed in the text. Taxon names are followed by sectional placement and distribution (in parentheses). The rhombus (◇) and star (☆) signs denote calibration points for molecular dating. Sectional classification and clade names in Thomas et al. (2011a) are marked to the right to allow easier cross-study comparison. Sources of sectional placement for each species are cited in Additional file1. Sectional abbreviations: ALI: Alicida, AUG: Augustia, BAR: Baryandra, COL: Coelocentrum, DIP: Diploclinium, HAA: Haagea, LEP: Leprosae, PAR: Parvibegonia, PET: Petermannia, PLA: Platycentrum, REI: Reichenheimia, RID: Ridleyella, SPH: Sphenanthera, SYM: Symbegonia, UA: unassigned.

Figure 2

Maximum clade credibility chronogram estimated by BEAST. The rhombus (◇) and star (☆) signs denote calibration points for molecular dating. Dashed clades indicate PP < 0.75 and thicken clades indicate PP ≥ 0.95. Node heights indicate mean ages, with 95% highest posterior density (HPD) date ranges shown by the node bars. Clades with PP ≥ 0.75 are numbered and their clade support and divergent ages mean (95% HPD) are shown in Table 2.