Reticulate evolution and sea‐level fluctuations together drove species diversification of slipper orchids (Paphiopedilum) inSouth‐EastAsia

Abstract

South-East Asia covers four of the world's biodiversity hotspots, showing high species diversity and endemism. Owing to the successive expansion and contraction of distribution and the fragmentation by geographical barriers, the tropical flora greatly diversified in this region during the Tertiary, but the evolutionary tempo and mode of species diversity remain poorly investigated. Paphiopedilum, the largest genus of slipper orchids comprising nearly 100 species, is mainly distributed in South-East Asia, providing an ideal system for exploring how plant species diversity was shaped in this region. Here, we investigated the evolutionary history of this genus with eight cpDNA regions and four low-copy nuclear genes. Discordance between gene trees and network analysis indicates that reticulate evolution occurred in the genus. Ancestral area reconstruction suggests that vicariance and long-distance dispersal together led to its current distribution. Diversification rate variation was detected and strongly correlated with the species diversity in subg. Paphiopedilum (~80 species). The shift of speciation rate in subg. Paphiopedilum was coincident with sea-level fluctuations in the late Cenozoic, which could have provided ecological opportunities for speciation and created bridges or barriers for gene flow. Moreover, some other factors (e.g. sympatric distribution, incomplete reproductive barriers and clonal propagation) might also be advantageous for the formation and reproduction of hybrid species. In conclusion, our study suggests that the interplay of reticulate evolution and sea-level fluctuations has promoted the diversification of the genus Paphiopedilum and sheds light into the evolution of Orchidaceae and the historical processes of plant species diversification in South-East Asia.

Iteration expansion and regional evolution: phylogeography of Dendrobium officinale and four related taxa in southern China

“…Reticulate evolution has been shown to be a driving force for species diversification via hybridization events41. In addition, transitions between self-compatibility (SC) and self-incompatibility (SI) can gradual accumulate genetic incompatibilities preventing gene flow among Dendrobium species42.…”

Taxonomic placement of Paphiopedilum rungsuriyanum (Cypripedioideae; Orchidaceae) based on morphological, cytological and molecular analyses

“…The phylogenetic analyses using multiple genes would be helpful in the treatment of systematic position at subgenus/section levels. For the study on the taxonomic position of P. rungsuriyanum , the present phylogenetic analyses are primarily conducted based on the molecular dataset published by Guo et al (2015). The results are consistent with the previous molecular studies (Chochai et al 2012; Gorniak et al 2014), indicating that the well-supported division of the genus Paphiopedilum into three subgenera Parvisepalum , Brachypetalum and Paphiopedilum .…”

“…The incongruence between plastid and nuclear gene trees may be caused by horizontal gene transfer, hybridization, and/or incomplete lineage sorting (Nishimoto et al 2003; Maddison and Knowles 2006; Kim and Donoghue 2008; Petit and Excoffier 2009; Yu et al 2013). In Paphiopedilum , based on the multiple low-copy nuclear genes and the network analyses, subgenus Paphiopedilum (particularly sections Barbata , Cochlopetalum and Paphiopedilum ) had a higher species diversification rate than the other subgenera of Paphiopedilum , suggesting that hybridization plays an important role in speciation (Guo et al 2015). Due to the lack of strong interspecific reproductive barriers in Paphiopedilum species, it is proposed that as the geographic and ecological changes (e.g.…”

“…The nuclear ribosomal spacer regions, ITS1 and ITS2, and the 5.8S ribosomal gene (ITS) (Douzery et al 1999), three low-copy nuclear genes ( ACO , DEF 4 and RAD 51) and four plastid regions ( atp I- atp H, matK , trn S- trn fM and ycf 1) were amplified with the same primers as in Guo et al (2015) and listed in Additional file 2: Table S2. PCR amplification and the Sanger sequencing were carried out as described by Guo et al (2015). PCR products that were difficult to sequence directly were cloned using the pGEM-T Vector System II (Promega, Madison, WI, USA).…”

“…For phylogenetic analysis, four low-copy nuclear genes ( ACO , DEF 4, ITS and RAD 51), four plastid regions ( atp I- atp H, matK , trn S- trn fM and ycf 1) and the combined all data were added to the analysis by referring the data matrices created by Guo et al (2015), and sequences of Mexipedium xerophyticum and Phragmipedium longifolium were used as outgroup taxa. DNA sequences were aligned using CLUSTALX (Thompson et al 1997), followed by manual adjustment.…”