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Melastoma Candidum and M. Sanguineum Extensive Hybridization and Introgression between Melastoma candidum and M. sanguineum Ting Liu1, Yunyun Chen2, Lifang Chao1, Shuqiong Wang1, Wei Wu3, Seping Dai4, Feng Wang5, Qiang Fan1, Renchao Zhou1* 1 State Key Laboratory of Biocontrol and Guangdong Key Laboratory of Plant Resources, Sun Yat-sen University, Guangzhou, China, 2 School of Pharmaceutical Sciences, Sun Yat-Sen University, Guangzhou, China, 3 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China, 4 Guangzhou Institute of Landscape Gardening, Guangzhou, China, 5 College of Pharmacy, Jinan University, Guangzhou, China Abstract Natural hybridization can lead to various evolutionary outcomes in plants, including hybrid speciation and interspecific gene transfer. It can also cause taxonomic problems, especially in plant genera containing multiple species. In this study, the hybrid status of Melastoma affine, the most widespread taxon in this genus, and introgression between its putative parental species, M. candidum and M. sanguineum, were assessed on two sites, Hainan and Guangdong, using 13 SSR markers and sequences of a chloroplast intergenic spacer. Bayesian-based STRUCTURE analysis detected two most likely distinct clusters for the three taxa, and 76.0% and 73.9% of the morphologically identified individuals of M. candidum and M. sanguineum were correctly assigned, respectively. 74.5% of the M. affine individuals had a membership coefficient to either parental species between 0.1 and 0.9, suggesting admixture between M. candidum and M. sanguineum. Furthermore, NewHybrids analysis suggested that most individuals of M. affine were F2 hybrids or backcross hybrids to M. candidum, and that there was extensive introgression between M. candidum and M. sanguineum. These SSR data thus provides convincing evidence for hybrid origin of M. affine and extensive introgression between M. candidum and M. sanguineum. Chloroplast DNA results were consistent with this conclusion. Much higher hybrid frequency on the more disturbed Guangdong site suggests that human disturbance might offer suitable habitats for the survival of hybrids, a hypothesis that is in need of further testing. Citation: Liu T, Chen Y, Chao L, Wang S, Wu W, et al. (2014) Extensive Hybridization and Introgression between Melastoma candidum and M. sanguineum. PLoS ONE 9(5): e96680. doi:10.1371/journal.pone.0096680 Editor: Joa˜o Pinto, Instituto de Higiene e Medicina Tropical, Portugal Received November 15, 2013; Accepted April 10, 2014; Published May 5, 2014 Copyright: ß 2014 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study is supported by grants from the National Natural Science Foundation of China (31170213 and 91231106), SRF for ROCS, SEM, and Chang Hungta Science Foundation of Sun Yat-sen University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction morphological traits can be observed. So keeping hybridization in mind should enable better decisions regarding taxonomic The roles of hybridization in plant evolution have been well treatment. recognized in the past few decades (reviewed in [1]). Interspecific Taxonomic problems are common in many plant genera with hybridization can lead to hybrid speciation by allowing adaptation multiple species. One such case is the genus Melastoma L. to extreme or novel habitats [2], reinforcement of premating (Melastomataceae). Melastoma is centered in Southeast Asia and isolation as a response to maladaptive hybridization [3,4], and extends to India, southern China, and northern Australia [13]. It adaptive gene transfer through introgression [5]. Thus, studies of was previously estimated that this genus comprises approximately hybridization are important for understanding interspecific 50–100 species [14,15], but only 22 species are recognized in the relationships and evolutionary processes. It is particularly inter- latest revision by Meyer [13]. Many species of Melastoma have a esting to study reproductive isolation in zones of hybridization and relatively high degree of overlap in geographic distributions and introgression, where species can maintain their identity in the face flowering periods [14], and largely shared pollinators [16–19], of extensive gene flow. Hybridizing species can exchange neutral offering ample opportunities for hybridization. Artificial crosses or adaptive alleles, while genes underlying local adaptation or have been successfully made between some species of Melastoma, related to reproductive isolation will be impeded [6]. Differential and the hybrids exhibit vigorous growth (S. Dai, unpublished introgression between hybridizing species, which refers to locus- data). Recently, we have identified Melastoma intermedium as a specific patterns of introgression across the genomes, offers natural hybrid between M. candidum and M. dodecandrum based on excellent opportunities to investigate the contribution of ecological sequences of two nuclear genes [11]. These results indicate that processes to speciation [7–9]. reproductive isolation between some Melastoma species is not Hybridization can also cause taxonomic problems. Interspecific complete. hybrids can have parental, intermediate and even novel traits [10], Three taxa of Melastoma, namely, M. affine, M. candidum and M. and they may be given the status of species, subspecies or just sanguineum, are very common and often sympatric in Southeast varieties by taxonomists (e.g. [11,12]). The situation is more M. candidum M. sanguineum complex in hybrid swarms, where a continuous range of Asia and southern China. and differ PLOS ONE | www.plosone.org 1 May 2014 | Volume 9 | Issue 5 | e96680 Hybridization and Introgression in Melastoma markedly in indumentums of leaf and hypanthium (a cup-shaped Materials and Methods structure which bears the sepals, petals, and stamens), which are the most important morphological traits for species delimitation in Plant Materials Melastoma, as mentioned by Meyer [13]. In habitat, M. candidum,a Our sampling sites were located in Baihualing Mountain, light demanding opportunist, often occurs in open fields, Qiongzhong, Hainan and Zhuhai Campus of Sun Yat-sen grasslands and roadsides. In contrast, M. sanguineum prefers shady University, Zhuhai, Guangdong. At both locations, no specific environments, and is usually found in the edge of forest permissions were required for scientific research. No endangered understory. M. affine, initially published as a new species [20], is or protected species were involved at the two locations. There is the most widely distributed taxon in this genus, ranging from little human disturbance in Baihualing Mountain area. Zhuhai southern China to northern Australia [13,14]. Together with M. Campus of Sun Yat-sen University was founded in 1999 and our candidum and M. normale, it was incorporated into M. malabathricum sampling site is located at the boundary of the secondary forest and in the English version of Flora of China [21]. As M. candidum and an ornamental lawn (Zoysia tenuifolia). At this site, the habitats have M. normale are in fact distinct species based on morphological, been severely disturbed because partial forests were removed for phenological and molecular data (T. Liu et al. unpublished data), the construction of the lawn, and shrubs and weeds are removed the taxonomic treatment is not reasonable and we will use the every year. For short, we will use Hainan and Guangdong for the species names for Melastoma in this study according to the Chinese two sites hereafter. On both sites, three taxa of Melastoma, namely, version of Flora of China [14]. M. affine has many morphological M. candidum, M. sanguineum and M. affine are common and traits intermediate between M. candidum and M. sanguineum sympatric. Plants were provisionally identified according to the (Figure 1). These morphologically intermediate traits in M. affine, diagnostic morphological characteristics described in the Chinese including trichomes in leaf, branchlet and hypanthium, leaf and version of Flora of China. Briefly, M. candidum has densely bract shape, show a continuous range, with two ends resembling puberulous trichomes in the leaves, and appressed scales on the those of M. candidum and M. sanguineum, respectively. It is branchlets and hypanthiums, while M. sanguineum has glabrous frequently found in disturbed habitats, where it is often more leaves and spreading, hispid trichomes on the branchlets and abundant than M. candidum and M. sanguineum. Based on its hypanthiums (Fig. 1). In addition, the two species differ strikingly morphological intermediacy and overlapping distribution with M. in leaf shape, with lanceolate leaves and five veins for M. candidum and M. sanguineum, we propose that M. affine might sanguineum, and elliptic to elliptic-ovate leaves and usually seven represent an interspecific hybrid between M. candidum and M. veins for M. candidum. M. affine has many intermediate morpho- sanguineum. A continuous range of morphological intermediacy logical traits, including trichomes in leaf, branchlet and hypanthi- suggests that introgression
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