Lineage diversification and hybridization in the Cayratia japonica–Cayratia tenuifolia species complex
Graphical abstract
Introduction
The Sino-Japanese floristic region in temperate Asia has remarkably rich biodiversity compared to other temperate floristic regions worldwide. The high species richness of the region is explained by its climatic diversity, complex topography, complex geological history, and the absence of major extinctions during Quaternary glaciations (Qian and Ricklefs, 2000, Harrison et al., 2001, Milne and Abbott, 2002, Milne, 2006, Qiu et al., 2011). Adjacent to temperate Asia, tropical Asia (Indo-Burma and Sundaland) is also known for high biodiversity (Myers et al., 2000). In addition to the high rates of endemics in these floristic regions, some species are widely distributed across the regions. Those species have previously received little attention; however, recent advances in molecular analyses have made it possible to reveal hidden lineages within a species (e.g., Qiu et al., 2011). Phylogeographic analyses of such species may reveal how they spread across floristic regions and help to clarify the geological histories of temperate and tropical Asia.
Cayratia Jussieu (Vitaceae) comprises over 60 species, occurring mainly in tropical and subtropical Asia, Africa, Australasia, and the Pacific islands (Wen, 2007, Lu et al., 2013). Cayratia japonica (Thunb.) Gagnep. is distributed from the temperate to tropical regions of East Asia, Southeast Asia, India, and Australia (Jackes, 1987, Ohba, 1999, Hui and Wen, 2007). Two intraspecific varieties are recognized in China: C. japonica var. pseudotrifolia (W.T. Wang) C.L. Li and C. japonica var. mollis (Wallich ex M.A. Lawson) Momiyama (Hui and Wen, 2007). Cayratia tenuifolia (Wight & Arn.) Gagnep. occurs in the Japanese islands of Kyushu and the Ryukyus, as well as in Taiwan, the Malay Peninsula, and Borneo. It was morphologically distinguished from C. japonica by differences in dentate leaflet margins (Hatusima and Amano, 1967, Hatusima, 1971) and was treated as a synonym of C. japonica var. dentata (Makino) Honda (Makino, 1909, Ohba, 1999). Okada et al. (2007) suggested that C. tenuifolia might be distinguished from C. japonica by differences in the color of the floral disc at anthesis: specifically, yellow in C. tenuifolia and orange in C. japonica.
The chromosome number of C. japonica has been reported as 2n = 40 in China (Huang et al., 1988). Both C. japonica and C. tenuifolia contain diploids (2n = 2x = 40) and triploids (2n = 3x = 60) in Japan (Okada et al., 2003, Okada et al., 2005, Okada et al., 2007, Tsukaya et al., 2012). Consistent with triploids in other species, the triploids of C. japonica and C. tenuifolia have low fertilities and rarely bear fruit. Moreover, the diploid C. japonica of Honshu, Japan, has variable pollen fertility (31–97%; Okada et al., 2003) and is often unable to produce seeds. Both C. japonica and C. tenuifolia readily propagate vegetatively, and thus some individuals of the species were assumed to spread through vegetative clones in Japan (Okada et al., 2003).
In a previous study, we explored the origins of triploids of C. japonica and C. tenuifolia in Japan using the single-copy nuclear gene ASYMMETRIC LEAVES 1 (AS1) (Tsukaya et al., 2012). According to the phylogenetic investigation, alleles were divided into three distinct lineages, the majority of which were shared by C. japonica and C. tenuifolia. These results suggested that the two species were not phylogeneticaly distinct from each other and may be members of a species complex (Tsukaya et al., 2012). In addition, the majority of diploids and all triploids were heterozygous for the AS1 genotypes and consisted of two alleles with distinct lineages, suggesting that lineage diversifications were followed by lineage admixtures through hybridizations. Furthermore, triploids of each species originated from independent hybridizations.
Only a few studies have examined this species complex in other regions. In Australia, C. japonica is found along the east coast of Queensland (Jackes, 1987). Although phylogenetic relationships between Australasian C. japonica and other Australian species of Vitaceae were investigated (Rossetto et al., 2001, Rossetto et al., 2007), the analysis did not include the Asian C. japonica. The phylogenetic relationship between C. japonica in Australia and Asia has not yet been examined.
In this study, we used expanded taxon sampling and additional molecular markers to determine the phylogenetic relationships among the C. japonica–C. tenuifolia species complex across most of its distribution. Details of divergences and hybridizations among major lineages were assessed. Divergence times of the main lineages and the ancestral area of the species complex were estimated, and the divergence history of this clade was also investigated. The species complex is widely distributed across temperate to tropical regions from East Asia to Australia and provides an appropriate model system for determining the origins of intraspecies complex lineages.
Section snippets
Materials and determinations of ploidy levels
Cayratia japonica and C. tenuifolia were treated as members of the C. japonica–C. tenuifolia species complex in the present study, as suggested by Tsukaya et al. (2012). We collected 116 accessions of the C. japonica–C. tenuifolia species complex from native habitats in Australia, China, Japan, Korea, Taiwan, Indonesia, Malaysia, and Myanmar (details of accessions are shown in Supplementary Table 1). Both C. japonica var. pseudotrifolia and C. japonica var. mollis were included (Supplementary
Haplotypes of cpDNA (trnL-F and trnC-petN) and phylogeny
Nucleotide sequences of trnL-F and trnC-petN were determined for 112 accessions (Supplementary Table 1). Four nucleotide sequences were obtained from GenBank (Supplementary Table 1, ID Nos. 112–115). In total, 27 unique trnL-F types (trnLF-1–trnLF-27) and 20 unique trnC-petN types (trnCpetN-1–trnCpetN-20) were identified. Accession numbers of these types are listed in Supplementary Table 3. The combined trnL-F and trnC-petN produced 34 unique haplotypes (HT1–HT34), which are provided in
Asian C. japonica–C. tenuifolia species complex
Phylogenetic analysis of cpDNA revealed a set of well-resolved and highly supported clades within the monophyletic Asian C. japonica–C. tenuifolia species complex (Fig. 1, e.g., CP1.1 and CP1.2). However, we observed no morphological distinctions among the lineages, and thus the diversification was cryptic. According to the AS1 analysis, the Asian lineage was divided into seven subclades (subclades A–G; Fig. 3). Four different heterozygous genotypes composed of two alleles in the different
Conclusions
We performed phylogenetic analysis of the C. japonica–C. tenuifolia species complex using the nuclear-encoded AS1 and two cpDNA loci. Three major conclusions emerged from this analysis. First, distinct monophyly of Asian and Australian lineages was determined (Fig. 1, Fig. 3). Second, two major lineages of cpDNA diverged in mid-continental Asia during the Tertiary (Clade-CP1.1 and Clade-CP1.2). The extrusion of Indochina from southeastern China during the Oligo–Miocene might have been
Acknowledgments
This study was supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science. We express our thanks to Dr. D. Li (Kunming Institute of Botany) for arranging our field study in Yunnan, China. We also thank the Secretariat of Permission for Foreign Research, the Ministry of Research and Technology, Republic of Indonesia (RISTEK), the Indonesian Institute of Science (LIPI), and the Betung Kerihun National Park office for allowing this study to take place
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