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Table of Content
    Volume 25 Issue 6
    20 June 2017

    Hybridization is a prevalent phenomenon in nature, which plays an important role in evolution. It can transfer adaptive genetic variation between divergent lineages and generate new genetic recombination, through genetic exchange, or even generate new hybrid species either through allopolyploid or homoploid hybrid speciation. Studying the evolutionary outcomes of hybridization will aid understanding of the impact of hybridization on generating and maintaining of biological diversity. The articles in this special issue on Natural Hybridization and Biodiversity provide new insights in the genomic era into the important evolutionary consequences of hybridization. (Designed by Shuai Nie, Wei Ba and Jianfeng Mao)

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    All Papers in This Issue
    Biodiv Sci. 2017, 25 (6):  0-0. 
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    Natural hybridization: a nightmare or a delight to biodiversity?
    Yuehong Yan, Ming Kang, Yongpeng Ma, Renchao Zhou
    Biodiv Sci. 2017, 25 (6):  561-564.  doi:10.17520/biods.2017180
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    Natural hybridization and speciation
    Yuguo Wang
    Biodiv Sci. 2017, 25 (6):  565-576.  doi:10.17520/biods.2017041
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    Natural hybridization plays a pivotal role in the formation of new species during the evolution of organisms. There are two principal types of hybrid speciation: polyploidization and homoploid hybrid speciation. The former has been regarded as an important force driving plant speciation, whereas the latter has proved to be a main mode of speciation based on an increasing number of cases, which have reported successful crosses between the species at the same ploidy level. However, only a few cases of homoploid hybrid speciation have been documented when strict criteria are applied. Therefore, molecular evidence involving more genomic loci and morphological investigations from different kinds of hybrid zones, as well as assessments of existing speciation models and new computer stimulations, are required for further understanding the genetic basis of the initial and entire process of speciation. Through the historical reconstruction of gene flow between diverging lineages, additional organismal models for hybrid speciation need to be developed to reveal the effects of natural selection on the formation of reproductive isolation, and to discern the ecologically adaptive changes and the formation rules of novel diversity in the process of hybrid speciation. Here I briefly review the history of studies examining natural hybridization and speciation to introduce concept changes, research methods, and the latest advances of natural hybridization and speciation, to identify the unsolved core and basic scientific questions and to provide feasible suggestions for future studies and the protection of biodiversity involved in natural hybridization.

    Approaches used to detect and test hybridization: combining phylogenetic and population genetic analyses
    Jian-Feng Mao, Yongpeng Ma, Renchao Zhou
    Biodiv Sci. 2017, 25 (6):  577-599.  doi:10.17520/biods.2017097
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    Hybridization among diverging (interspecific or intraspecific) groups involves gene flow and genetic recombination. Increasingly, studies have shown that hybridization, a process of genetic exchanges, occurs widely in the divergence and unity of animals, plants, and microorganisms, and acts as an important mechanism for the formation and maintenance of biological diversity. The rapid development of high-throughput sequencing technology and the widespread application of genome-level techniques provides an unprecedented opportunity for us to further evaluate the universality and evolutionary significance of hybridization. However, selecting appropriate research techniques and strategies to detect the potential hybridization and evaluate its characteristics becomes a common question. In this review, we attempt to synthesize methods from phylogenetics and population genetics of the genomic era to provide biodiversity and evolutionary researchers a practical reference for testing hybridization.

    The roles of epigenetic variation in plant hybridization and polyploidization
    Linfeng Li, Bao Liu
    Biodiv Sci. 2017, 25 (6):  600-607.  doi:10.17520/biods.2017028
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    Hybridization and polyploidization are common phenomena in plants and play important roles in speciation and diversification of extant species. Previous studies using ecological, physiological and molecular investigations have provided a framework for understanding the underlying mechanisms of plant hybridization and polyploidization. In this review, we examine the roles of epigenetic variation in species evolution from an evolutionary perspective. We summarize recent advances in Arabidopsis thaliana, Oryza sativa and species of Brassica to elucidate the correlations between phenotypic novelty and epigenetic variation. Based on currently available observations, we propose that future studies should emphasize the roles of epigenetic variation at both the natural population and species levels, and that statistical methods need to be improved to identify causative epigenetic variations at the genome-wide level.

    Original Papers
    Reproductive isolation in sympatric Salvia species sharing a sole pollinator
    Yukun Wei, Yanbo Huang, Guibin Li
    Biodiv Sci. 2017, 25 (6):  608-614.  doi:10.17520/biods.2017039
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    Reproductive isolation (RI) is one of the key factors for speciation and diversity maintenance, however, there are differences in formation stage, means, and strength of RI for different species. To assess the effects and the significance of reproductive isolation in Salvia species, we compared flowering, pollination, and reproduction characteristics of Salvia liguliloba and S. bowleyana, which grow sympatrically and have overlapping flowering periods in the Tianmu Mountain, Zhejiang. Furthermore, artificial hybridization between the two species were conducted to estimate and understand their genetic compatibility and reproductive isolation. Results indicated that the two Salvia species considerably differed in their flower morphological structures, inflorescence organization, and the number of flowers produced per inflorescence. Bombus trifasciatus is the sole pollinator for these two species during the overlapping flowering period. However, different visitation behavior and floral structure (P < 0.05) leads to obviously different pollination patterns between the two species. Pollen is deposited on distinctly separate areas of the pollinator’s body in a manner precluding contact with any heterospecific Salvia stigmata. Under natural condition, the two species are equally successful in reproduction (natural seed set > 87%). Artificial pollination and hybridization experiments between these two species showed that they have a higher genetic compatibility. The cross seed sets are 77.8 ± 10.7% and 78.7 ± 11.2% when the two species are reciprocally cross parents. Our research suggests that for the two Salvia species lacking genetic incompatibility systems and relying on pollinators for outcrossing, there are differences in floral structures and pollen placement sites. The mechanical isolation (a form of pre-pollination RI) prevents heterospecific pollen interference and natural hybridization of the two different species that grow sympatrically and have overlapping flowering periods, and also maintains species diversity and the constancy of species heredity.

    Post-pollination reproductive isolation of sympatric populations of Primulina eburnea and P. mabaensis (Gesneriaceae)
    Xiaolong Zhang, Lihua Yang, Ming Kang
    Biodiv Sci. 2017, 25 (6):  615-620.  doi:10.17520/biods.2017029
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    Reproductive isolation is essential for sympatric populations of closely related species to maintain species integrity and to prevent genetic introgression caused by hybridization. Primulina is the largest genus of Gesneriaceae in China, with a high degree of species diversity and endemism. Most species of the genus are karst habitat specialists (i.e. calciphiles), and many closely related species show a sympatric distribution in karst landscapes. To better understand the mechanism of sympatry in Primulina, post-pollination reproductive isolation, including pollen competition, fruit set, seed mass, seed germination, and pollen viability, was investigated in two closely related species, P. eburnea and P. mabaensis. Results indicated that the total post-pollination isolation strength for P. eburnea and P. mabaensis was 0.09 and 0.13, respectively, which were not strong enough to prevent hybridization completely. The strength of reproductive isolation from pollen competition and seed germination of P. eburnea and P. mabaensis was negative, suggesting facilitation for gene flow between species; while the strength of the fruit set, seed mass, and pollen viability showed a weak role in preventing interspecies hybridization. However, the two species are able to maintain their integrity well, as rare hybrid individuals are found in nature, suggesting that the existence of pre-pollination isolation mechanisms may play a more important role in maintaining species boundaries in these two species.

    Polyploidy and the formation of species diversity in Aspleniaceae
    Yanfen Chang
    Biodiv Sci. 2017, 25 (6):  621-626.  doi:10.17520/biods.2017117
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    Ferns are considered to have the highest frequency of polyploidy in plants. Based on the published cytological data of 188 species, we analyzed the relationship between polyploidy and the formation of species diversity in the fern family Aspleniaceae, which comprises approximately 800 species. The results show that polyploids, including triploids, tetraploids, hexaploids, octoploids, decaploids, dodecaploids and hexadecaploids, have been documented in the family. Of the 188 Aspleniaceae species with cytological data, 88.8% exhibit polyploidy, 41.0% show intraspecific polyploidy and 47.9% are the result of polyploid speciation. In addition, the diverse ploidy levels suggest that these species have a complex evolutionary history and their taxonomic problems require further study. The perplexity and future directions of study of Aspleniaceae were also discussed.

    Molecular and morphological evidence for natural hybridization between Rhododendron decorum and R. delavayi (Ericaceae)
    Shuoli Zheng, Xiaoling Tian, Chengling Huang, Lingjun Wang, Yuan Feng, Jingli Zhang
    Biodiv Sci. 2017, 25 (6):  627-637.  doi:10.17520/biods.2017090
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    The southwestern region of China is the center of differentiation for the genus Rhododendron. Studies on the natural hybridization of Rhododendron provide solutions for taxonomic problems and enhance the ability to breed new cultivars faster. In this paper, we compared the morphological features and sequenced nuclear internal transcribed spacer (ITS) and chloroplast trnL-trnF, rbcL, trnH-psbA for Rhododendron decorum, R. delavayi, and the putative hybrid offspring of these two species. All samples in this study were collected from Baili Rhododendron Nature Reserve in Guizhou Province, the Shibao Mountain of Yunnan Province and Kunming Botanical Garden. Results showed that all putative hybrids (natural and artificial) produced an intermediate morphology. Sequencing results revealed that all artificial hybrids and one collected from the Shibao Mountain inherited cpDNA from R. decorum, and all putative hybrids collected from Baili Rhododendron Nature Reserve and six from Shibao Mountain inherited cpDNA from R. delavayi. In this study, we have confirmed that natural hybridization between R. decorum and R. delavayi exists in the Guizhou and Yunnan sites. Hybridization was bilateral, and most of the hybrids were derived from maternal parent R. delavayi.

    Molecular evidence for natural hybridization between two Melastoma species endemic to Hainan and their widespread congeners
    Qiujie Zhou, Yacheng Cai, Wei Lun Ng, Wei Wu, Seping Dai, Feng Wang, Renchao Zhou
    Biodiv Sci. 2017, 25 (6):  638-646.  doi:10.17520/biods.2017060
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    Natural hybridization plays an important role in speciation, genetic exchange, and adaptive evolution. However, it can also lead to the extinction of rare species or can generate super invasive species. Studies of natural hybridization involving rare species can therefore provide valuable information for species protection. In Melastoma, M. penicillatum and M. dendrisetosum are endemic to Hainan, China. M. dendrisetosum is at the edge of extinction, with a wild population of less than 300 individuals. Based on morphological observations during our field survey, we found that there are putative hybrids formed between the two endemic species and their widespread congeners, i.e. M. candidum × M. penicillatum and M. sanguineum × M. dendrisetosum. In this study, we sequenced four low-copy nuclear genes and five chloroplast DNA intergenic spacers of the putative hybrids and their putative parents. We found that these putative hybrids showed chromatogram signal additivity between putative parental species on differentially fixed sites at these nuclear genes. Haplotype networks also showed that at all four nuclear loci analyzed, alleles of the putative hybrids were shared with those of their putative parental species. The results above confirmed that hybridization occurred between M. candidum and M. penicillatum, and between M. sanguineum and M. dendrisetosum. Also, we found an extremely low level of genetic diversity in M. dendrisetosum relative to the three other species of Melastoma. It appears that there are strong ecological isolation between M. candidum and M. penicillatum as well as between M. sanguineum and M. dendrisetosum, and habitat disturbance caused by highway construction may have promoted hybridization between these species. Therefore, the key to protecting these two species endemic to Hainan is to reduce habitat disturbance. Artificial propagation of the species is another possible way to expand their population sizes.

    Asymmetric hybridization of Primula secundiflora and P. poissonii in three sympatric populations
    Yanping Xie, Jianli Zhao, Xingfu Zhu, Li Li, Qingjun Li
    Biodiv Sci. 2017, 25 (6):  647-653.  doi:10.17520/biods.2017001
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    Natural hybridization is one of the research hotspots in evolutionary biology. The direction of hybridization is a critical aspect to understanding natural hybridization and interspecific reproductive isolation. Although natural hybridization between Primula secundiflora and P. poissonii has been confirmed in overlapping areas in the Hengduan Mountains, the interspecific hybridization directions among different populations remain unclear. We chose three sympatric populations to test interspecific hybridization directions. Biparentally inherited nuclear internal transcribed spacer (ITS) and maternally inherited chloroplast sequence trnH-psbA techniques were used to confirm hybridization and to test directions. Moreover, hand pollination of intraspecies and interspecies populations were performed to detect which factors influence seed numbers and hybridization patterns. Results of DNA marker analysis suggested that the direction of hybridization was asymmetric in each population, and P. poissonii was found to be the most maternal parent. Intraspecific crossing produced significantly more seeds than interspecific crossing. Primula poissonii produced significantly higher seed numbers when it was treated as the maternal parent. The asymmetric direction may be the result of the asymmetric strength of reproductive barriers between P. secundiflora and P. poissonii. Similar mechanisms of reproductive isolation may contribute to the asymmetric hybridization among the three sympatric sites.

    Occurrence and characteristics of natural hybridization in Begonia in China
    Daike Tian, Chun Li, Yan Xiao, Naifeng Fu, Yi Tong, Ruijuan Wu
    Biodiv Sci. 2017, 25 (6):  654-674.  doi:10.17520/biods.2017050
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    Natural hybridization is a very common phenomenon in plants and has continuously been a hotspot in the scientific research of speciation and evolution. As one of the largest genera in plants, Begonia has a large number of species. However, very few cases have been reported on its natural hybrids. A systematic investigation of natural hybridization of Begonia can not only improve understanding of plant diversity and germplasm resources of this genus, but also be a step towards solving its taxonomical issues. Through a comprehensive field survey and experimental analysis of natural hybridization in Chinese begonias, we found nearly 50 populations of 31 natural hybrids occurred among 29 species, accounting for 15% of currently about 200 accepted species. Begonia hemsleyana and B. longifolia had the highest cross frequency and crossed with 8 and 7 other species, respectively. B. palmata contributed to 16 hybrid populations, the largest number in all individual species. The largest number of hybrids (31 hybrid populations from 20 parental species) occurred in Yunnan (mainly in the southern areas), followed by Taiwan and Guangxi. Hybridization between species was unidirectional in most cases, and the majority of hybrids were F1 individuals, which still rely on parents or hybridization zones and have not been established as a true species. Field observations showed that aphid flies, followed by members of the bee family (Apidae), were the most frequent visitors of begonia flowers, however, further studies are necessary to examine their behavior and the efficiency of pollination. The natural hybrids and their putative parents were identified using integrative methods of morphology, molecular research, and artificial crossing experiments. Genome size (C value) of hybrids was usually equal or close to the average of that of the two parents, with an error less than 10%, which could assist identification of hybrids and parents. In addition, we summarized the five conditions necessary for the occurrence of natural hybridization: overlapping or adjacent distributions, concurrent flowering (at least partially overlapping), efficient pollination media, cross compatibility, and suitable microhabitat and climate conditions for seed germination and seedling growth. Based on these, we also predicted future putative parents of about 40 new natural hybrids and possible hybridization sites. Thus far, although all the known natural begonia hybrids have not established as true species, it may be more appropriate to treat them as a special taxon of speciation and evolution, which should be thoroughly investigated and published referring to protocols for publishing a new taxon in the scientific research. Because the individuals of natural hybrids in Begonia are always sparsely distributed in small numbers, and hybrids are not harmful to its parents it increases plant diversity and the chances of obtaining a new ornamental cultivar by natural selection. Therefore, the priority of in situ conservation should be given to regions with natural hybrids and species-rich environments. Meanwhile, for the purpose of ex situ conservation, requiring sufficient planting distance between species should be considered in those species with overlapping flowering time to avoid possible natural hybridization due to high cross-compatibility, particularly in native begonias.

    The complex reticulate evolutionary relationships of early terrestrial plants as revealed by phylogenomics analysis
    Jiangping Shu, Li Liu, Hui Shen, Xiling Dai, Quanxi Wang, Yuehong Yan
    Biodiv Sci. 2017, 25 (6):  675-682.  doi:10.17520/biods.2017042
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    Plants from aquatic to terrestrial ecosystems have undergone a very complex evolution, and their evolutionary pathways of large numbers of genes may be different from one another, so that traditional phylogenetic trees cannot show true evolutionary relationships. The phylogenetic network graph is a good solution to show the complex relationships of reticulate evolution, including vertical evolution and horizontal evolution. In this paper, we selected Chlamydomonas reinhardtii and four terrestrial plants, and screened 1,668 one-to-one orthologous genes to reconstruct the phylogenetic relationship of terrestrial plants based on phylogenomics. Results showed that phylogenetic trees were different based on different analysis strategies. The 1,668 genes were analyzed separately and 15 different topologies were found. The phylogenetic network of the orthologous genes obtained from the five species was analyzed, and the results showed that in a very robust phylogenetic network map, only five species have nine different split branches, suggesting a very complex evolutionary relationship network. Futhermore, the difference in split branches between algae and bryophytes or lycophytes is very small, which may be one of the reasons influencing the phylogenetic tree conflict, and implies that early terrestrial plants underwent a complex radiate evolution.

    Natural hybridization and biodiversity conservation
    Hui Shang, Yuehong Yan
    Biodiv Sci. 2017, 25 (6):  683-688.  doi:10.17520/biods.2017122
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    Hybridization occurs commonly in nature. Due to decreasing fitness, a large number of hybridized offspring might be eliminated in natural conditions, but many hybridization/introgression events can be important drivers of speciation. With advances in modern molecular genotyping methods, the mechanisms of hybridization and their impacts on speciation are becoming better understood. However, for taxa with hybridized origins, the question of whether the germplasm needs to be conserved presents many viewpoints. Here, we comprehensively review the conservation value of hybrids over three aspects (including genetic diversity, species diversity, and ecosystem diversity) to pronounce the significant roles in evolution and ecology. A large number of cases indicate that not all hybridization will lead to genetic assimilation by hybridization swamping. It can also boost genetic diversity and increase fitness and adaptability. Based on recent research on natural hybridization, we propose a principle for conservation of hybridized originated taxa if the existing hybridized taxon does not threaten the parental species, and its unique germplasm can contribute to genetic and adaptive capacity. In such a situation, the conservation of hybridized taxa should be taken into consideration. We hope this proposal could supplement a reference to reinforce conservation policy and species red listing.

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