Biodiversity Science ›› 2017, Vol. 25 ›› Issue (6): 638-646.doi: 10.17520/biods.2017060

• Original Papers • Previous Article     Next Article

Molecular evidence for natural hybridization between two Melastoma species endemic to Hainan and their widespread congeners

Qiujie Zhou1, Yacheng Cai1, Wei Lun Ng1, Wei Wu1, Seping Dai2, Feng Wang3, Renchao Zhou1, *()   

  1. 1 School of Life Sciences, Sun Yat-sen University, Guangzhou 510275
    2 Guangzhou Institute of Forestry and Landscape Architecture, Guangzhou 510520
    3 College of Pharmacy, Jinan University, Guangzhou 510632
  • Received:2017-02-27 Accepted:2017-04-12 Online:2017-07-10
  • Zhou Renchao E-mail:zhrench@mail.sysu.edu.cn

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.

Key words: Melastoma, natural hybridization, endangered species, nuclear genes, chloroplast intergenic spacer, conservation

Fig. 1

Morphological comparison between Melastoma penicillatum, M. candidum and their putative hybrid. (A) M. penicillatum, (B) putative hybrid, (C) M. candidum. Fruits of M. penicillatum (D), putative hybrid (E) and M. candidum (F)."

Fig. 2

Morphological comparison between Melastoma dendrisetosum, M. sanguineum and their putative hybrid. Fruits of M. dendrisetosum (A), putative hybrid (B) and M. sanguineum (C). D, Leaves of M. dendrisetosum (left), putative hybrid (middle) and M. sanguineum (right). E, Young twigs of M. dendrisetosum (left), putative hybrid (middle) and M. sanguineum (right)."

Table 1

Sampling details of four species of Melastoma and two putative hybrids used in this study"

类群 Taxon 采样地点 Location 个体数量 Sample size
野牡丹 M. candidum (Cf) 福建龙海 Longhai, Fujian 19
野牡丹 M. candidum (Ch) 海南吊罗山 Diaoluoshan, Hainan 20
毛菍 M. sanguineum (S) 海南吊罗山 Diaoluoshan, Hainan 20
紫毛野牡丹 M. penicillatum (P) 海南吊罗山 Diaoluoshan, Hainan 20
枝毛野牡丹 M. dendrisetosum (D) 海南吊罗山 Diaoluoshan, Hainan 20
紫毛野牡丹与野牡丹的嫌疑杂种 Putative hybrid between P and C 海南吊罗山 Diaoluoshan, Hainan 1
枝毛野牡丹与毛菍的嫌疑杂种 Putative hybrid between D and S 海南吊罗山 Diaoluoshan, Hainan 4

Table 2

The base composition of the differentially fixed sites at the cam and tpi genes between Melastoma penicillatum and M. candidum in their putative hybrid (R = A + G; Y = C + T; W = T + A)"

类群 Taxon cam tpi
292 244 204 225 258 272 315 340 568
野牡丹 Melastoma candidum (C) A G T T T G A T C
紫毛野牡丹 M. penicillatum (P) G A A C C A G C T
紫毛野牡丹和野牡丹的嫌疑杂种 Putative hybrid between P and C R R W Y Y R R Y Y

Table 3

The base composition of the differentially fixed sites at the four nuclear genes between Melastoma dendrisetosum and M. sanguineum in their putative hybrid (R = A + G; Y = C + T; W = T + A; M = A + C; S = C + G)"

类群 Taxon cam chi gbss tpi
190 329 661 79 258 315 414 80 240 286
毛菍 M. sanguineum (S) T C G C A G G G T A
枝毛野牡丹 M. dendrisetosum (D) C T A T C A C A C T
枝毛野牡丹和毛菍的嫌疑杂种 Putative hybrid between D and S Y Y R Y M R S R Y W

Fig. 3

Median-joining networks of tpi (A), gbss (B), chi (C) and cam (D) genes of the four Melastoma species and the two putative hybrids. The numbers around the connecting lines between haplotypes represent the number of mutational steps between them, while those without numbers represent only one mutational step. Small black circles represent hypothetical or unsampled haplotypes."

Table 4

Genotypes of two putative hybrids of Melastoma at four nuclear genes (tpi, cam, chi and gbss). Haplotypes with single, double, wavy, or dotted underlines have identical sequences with those of M. candidum, M. penicillatum, M. sanguineum, and M. dendrisetosum, respectively. Haplotypes without underline are unique to the putative hybrids."

类群 Taxon 个体编号 Sample ID tpi cam chi gbss
紫毛野牡丹和野牡丹的嫌疑杂种 Putative hybrid (PC) PC PC1PC2 PC1PC2 PC1PC2 PC1 PC2
枝毛野牡丹和毛菍的嫌疑杂种
Putative hybrid (DS)
DS_1 DS1DS2 DS1DS4 DS1 DS2 DS1DS2
DS_2 DS1DS3 DS2DS4 DS1DS3 DS3DS4
DS_3 DS1DS4 DS3DS5 DS3DS4 DS1DS2
DS_4 DS1DS5 DS2DS4 DS1DS3 DS1DS5
[1] Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R, Dieckmann U, Eroukhmanoff F, Grill A, Cahan SH, Hermansen JS, Hewitt G, Hudson AG, Jiggins C, Jones J, Keller B, Marczewski T, Mallet J, Martinez-Rodriguez P, Möst M, Mullen S, Nichols R, Nolte AW, Parisod C, Pfennig K, Rice AM, Ritchie MG, Seifert B, Smadja CM, Stelkens R, Szymura JM, Väinölä R, Wolf JBW, Zinner D, Butlin RK (2013) Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
[2] Arnold ML (1997) xNatural Hybridization and Evolution. Oxford University Press, Oxford.
[3] Arnold ML (2006) Evolution Through Genetic Exchange. Oxford University Press, Oxford.
[4] Arnold ML, Martin NH (2009) Adaptation by introgression. Journal of Biology, 8, 82.
[5] Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
[6] Chao LF, Chen YY, Wang SQ, Liu T, Wu W, Dai SP, Wang F, Fan Q, Shi SH, Zhou RC (2014) One species or two? Multilocus analysis of nucleotide variation of Melastoma penicillatum and Melastoma sanguineum (Melastomataceae) in Hainan, China. Biochemical Systematics and Ecology, 55, 275-282.
[7] Chen J, Renner SS (2007) Melastomataceae. In: Flora of China (ed. Editorial Committee of Flora of China), Vol. 13, pp. 360-399. Science Press, Beijing and Missouri Botanical Garden, St Louis.
[8] Chen J (1983) A study of Melastoma (Melastomataceae) in China. Journal of South China Agricultural College, 4(1), 31-36.
(in Chinese) [陈介 (1983) 中国野牡丹科野牡丹属植物的研究. 华南农学院学报, 4(1), 31-36.]
[9] Chen J (1984) Melastomataceae. In: Flora Reipublicae Popularis Sinicae (ed. Editorial Committee of Flora Reipublicae Popularis Sinicae, Chinese Academy of Sciences), Tomus, 53(1), pp. 152-161. Science Press, Beijing.
(in Chinese) [陈介 (1984) 野牡丹科. 见: 中国植物志 (中国科学院中国植物志编辑委员会编), 53(1), 152-161. 科学出版社, 北京.]
[10] Dai SP, Wu W, Zhang RS, Liu T, Chen YY, Shi SH, Zhou RC (2012) Molecular evidence for hybrid origin of Melastoma intermedium. Biochemical Systematics and Ecology, 41, 136-141.
[11] Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19, 11-15.
[12] Grant PR, Grant BR (2014) Speciation undone. Nature, 507, 178-179.
[13] Gross CL (1993) The breeding system and pollinators of Melastoma affine (Melastomataceae): a pioneer shrub in tropical Australia. Biotropica, 25, 468-474.
[14] Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biological Conservation, 89, 143-152.
[15] Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451-1452.
[16] Liu T, Chen YY, Chao LF, Wang SQ, Wu W, Dai SP, Wang F, Fan Q, Zhou RC (2014) Extensive hybridization and introgression between Melastoma candidum and M. sanguineum. PLoS ONE, 9, e96680.
[17] Lu GH, Wu WH, Wang RZ, Li XL, Wang YQ (2009) Division of labor of heteromorphic stamens in Melastoma malabathricum. Biodiversity Science, 17, 174-181. (in Chinese with English abstract)
[路国辉, 武文华, 王瑞珍, 李新亮, 王英强 (2009) 野牡丹异型雄蕊的功能分化. 生物多样性, 17, 174-181.]
[18] Luo ZL, Zhang DX (2005) A review of heteranthery in flowering plants. Journal of Tropical and Subtropical Botany, 13, 536-542.
[19] Luo ZL, Zhang DX, Renner SS (2008) Why two kinds of stamens in buzz-pollinated flowers? Experimental support for Darwin’s division-of-labour hypothesis. Functional Ecology, 22, 794-800.
[20] Luo ZL, Gu L, Zhang DX (2009) Intrafloral differentiation of stamens in heterantherous flowers. Journal of Systematics and Evolution, 47, 43-56.
[21] Mallet J (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229-237.
[22] Meyer K (2001) Revision of the Southeast Asian genus Melastoma. Blumea, 46, 351-398.
[23] Moody ML, Les DH (2002) Evidence of hybridity in invasive watermilfoil (Myriophyllum) populations. Proceedings of the National Academy of Sciences, USA, 99, 14867-14871.
[24] Peng DH, Lan SR, Wu SS (2014) Pollination biology and breeding system of Melastoma dendrisetosum. Forest Research, 27(1), 11-16. (in Chinese with English abstract)
[彭东辉, 兰思仁, 吴沙沙 (2014) 中国特有种枝毛野牡丹传粉生物学及繁育系统研究. 林业科学研究, 27(1), 11-16.]
[25] Renner SS, Meyer K (2001) Melastomeae come full circle: biogeographic reconstruction and molecular clock dating. Evolution, 55, 1315-1324.
[26] Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics, 27, 83-109.
[27] Rieseberg LH (1997) Hybrid origins of plant species. Annual Review of Ecology and Systematics, 28, 359-389.
[28] Strand AE, Leebens-Mack J, Milligan BG (1997) Nuclear DNA-based markers for plant evolutionary biology. Molecular Ecology, 6, 113-118.
[29] Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology, 17, 1105-1109.
[30] Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25, 4876-4882.
[31] Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S, Heredia SM, Hahn MA, Caseys C, Bock DG, Rieseberg LH (2016) Hybridization and extinction. Evolutionary Applications, 9, 892-908.
[32] Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conservation Biology, 15, 1039-1053.
[1] Jiang Zhigang. China’s key protected species lists, their criteria and management [J]. Biodiv Sci, 2019, 27(6): 698-703.
[2] Zhang Xiaoling, Li Yichao, Wang Yunyun, Cai Hongyu, Zeng Hui, Wang Zhiheng. Influence of future climate change in suitable habitats of tea in different countries [J]. Biodiv Sci, 2019, 27(6): 595-606.
[3] Mo Zhangqin. Re-legalizing China’s ecological conservation redline: The position, dilemma and path [J]. Biodiv Sci, 2019, 27(3): 347-352.
[4] Zhao Yang,Wen Yuanyuan. Development of Convention on Biological Diversity’s Global Platform for Business & Biodiversity: Policy suggestion for China [J]. Biodiv Sci, 2019, 27(3): 339-346.
[5] Lü Zhongmei. Systematic legislation for nature conservation with national parks as the main body [J]. Biodiv Sci, 2019, 27(2): 128-136.
[6] Xian Yang, Dong Xin, Xie Xiaoman, Wu Dan, Han Biao, Wang Yan. Effect of Conservation Conditions on Restricting Conservation of Acer rubrum cv. ‘Somerset’ [J]. Chin Bull Bot, 2019, 54(1): 64-71.
[7] Dong-Ting ZOU, Qing-Gang WANG, Ao LUO, Zhi-Heng WANG. Species richness patterns and resource plant conservation assessments of Rosaceae in China [J]. Chin J Plant Ecol, 2019, 43(1): 1-15.
[8] Wang Yufei,Su Hongqiao,Zhao Xinrui,Su Yang,Luo Min. Conservation easement-inspired adaptive management methods for natural protected areas: A case study on Qianjiangyuan National Park pilot [J]. Biodiv Sci, 2019, 27(1): 88-96.
[9] Zhiyao Tang, Minwei Jiang, Jian Zhang, Xinyue Zhang. Applications of satellite and air-borne remote sensing in biodiversity research and conservation [J]. Biodiv Sci, 2018, 26(8): 807-818.
[10] Xuehua Liu, Pengfeng Wu, Xiangbo He, Xiangyu Zhao. Application and data mining of infra-red camera in the monitoring of species [J]. Biodiv Sci, 2018, 26(8): 850-861.
[11] Wang Shitong, Wu Hao, Liu Mengting, Zhang Jiaxin, Liu Jianming, Meng Hongjie, Xu Yaozhan, Qiao Xiujuan, Wei Xinzeng, Lu Zhijun, Jiang Mingxi. Community structure and dynamics of a remnant forest dominated by a plant species with extremely small population (Sinojackia huangmeiensis) in central China [J]. Biodiv Sci, 2018, 26(7): 749-759.
[12] Pei Yang,Yanqiong Peng,Ronghua Zhao,Darong Yang. Biological characteristics, threat factors and conservation strategies for the giant honey bee Apis dorsata [J]. Biodiv Sci, 2018, 26(5): 476-485.
[13] Jiaxing Huang,Jiandong An. Species diversity, pollination application and strategy for conservation of the bumblebees of China [J]. Biodiv Sci, 2018, 26(5): 486-497.
[14] Xiangyu Jia,Bin Bai,Jieqing Zhang,Yi Huang. The effects of IPBES deliverables on global biodiversity conservation strategy—an analysis based on the U. S. pollinator protection policy [J]. Biodiv Sci, 2018, 26(5): 527-534.
[15] Yao Zhao,Gengyun Li,Ji Yang. Conservation and utilization of wild relatives of cultivated plants [J]. Biodiv Sci, 2018, 26(4): 414-426.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Tao Yan, Tiantian Qu, Huanhuan Song, Philippe Ciais, Shilong Piao, Zhenzhong Sun and Hui Zeng. Contrasting effects of N addition on the N and P status of understory vegetation in plantations of sapling and mature Larix principis-rupprechtii[J]. J Plant Ecol, 2018, 11(6): 843 -852 .
[2] Zhigang Jiang,Yong Ma,Yi Wu,Yingxiang Wang,Zuojian Feng,Kaiya Zhou,Shaoying Liu,Zhenhua Luo,Chunwang Li. China’s mammalian diversity[J]. Biodiv Sci, 2015, 23(3): 351 -364 .
[3] Li Liang-Qian. On Distributional Features of the Genus Aconitum in Sino-Himalayan Flora[J]. J Syst Evol, 1988, 26(3): 189 -204 .
[4] Li Zhong-Ming. Palaeosmunda Emended and Two New Species[J]. J Syst Evol, 1983, 21(2): 153 -160 .
[5] Wei Zhou,Xu Li,Kaiyuan Li,Minghui Li. Fish faunal presence value in three first level tributaries of the Salween River in Yunnan, China and its meaning for aquatic nature reserve plan- ning[J]. Biodiv Sci, 2016, 24(10): 1146 -1153 .
[6] SUN Cheng-Ren. Micromorphological features of the seed surface of Schisandraceae and their systematic significance[J]. J Syst Evol, 2002, 40(2): 97 -109 .
[7] You Wen-hui, Song Yong-chang. A Study on Energy in Vascular Aquatic Macrophyte Communities in Dianshan Lake[J]. Chin J Plan Ecolo, 1995, 19(3): 208 -216 .
[8] Chunming Yuan,Yunfen Geng,Yong Chai,Jiabo Hao,Tao Wu. Response of lianas to edge effects in mid-montane moist evergreen broad- leaved forests in the Ailao Mountains, SW China[J]. Biodiv Sci, 2016, 24(1): 40 -47 .
[9] HE Wei-Ming and ZHONG Zhang-Cheng. Effects of Soil Fertility on Gynostemma pentaphyllum Makino Population Behavior[J]. Chin Bull Bot, 1999, 16(04): 425 -428 .
[10] CUI Xiao-Yong, Du Zhan-Chi, Wang Yan-Fen. Photosynthetic Characteristics of a Semi-arid Sandy Grassland Community in Inner Mongolia[J]. Chin J Plan Ecolo, 2000, 24(5): 541 -546 .