Biodiversity Science ›› 2019, Vol. 27 ›› Issue (11): 1196-1204.doi: 10.17520/biods.2019146

• Original Papers • Previous Article     Next Article

One or more species? GBS sequencing and morphological traits evidence reveal species diversification of Sphaeropteris brunoniana in China

Morigengaowa 1, 2, Hui Shang1, Baodong Liu2, Ming Kang3, Yuehong Yan1, *()   

  1. 1 Shanghai Chenshan Botanical Garden; Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai 201602
    2 Key Laboratory of Plant Biology, College of Heilongjiang Province, Harbin Normal University, Harbin 150025
    3 Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650
  • Received:2019-04-29 Accepted:2019-06-29 Online:2020-01-17
  • Yan Yuehong E-mail:yan.yh@126.com

Species are not static, but in the process of continuous differentiation and evolution. In this context, reproductive isolation is considered the key to most speciation events. However, species that may be only partially reproductively isolated may disturb our understanding of a species, as stated by ‘The integrative species concept’. In the Flora of China, Chinese Sphaeropteris contains two species, S. brunoniana and S. lepifera. S. brunoniana is thought to be the same species as a Hainan native, S. hainanensis, however, S. hainanensis seems to have differentiated morphologically. This study further explores the genetic relationship between S. brunoniana and its related species by collecting 21 samples from 9 populations for GBS reduced-representation genome sequencing for phylogenetic analysis. Using both genetic and morphological data, our results indicate that S. hainanensis differs genetically from S. brunoniana, but is also morphologically distinct based on leaf characteristics and spore ornamentation. Although the reproductive isolation of the two populations is weak, hybrids are formed in the coastal areas of Guangxi and leaves mimic intermediate morphology between parents. Therefore, our results suggest that S. hainanensis is in the process of speciation due to geographic isolation and suggests to restore its species status. S. brunoniana × hainanensis which the sample from Guangxi should be considered an independent natural hybrid taxon.

Key words: Sphaeropteris, S. hainanensis, speciation, natural hybridization, GBS, SNP

Table 1

Sample details of Sphaeropteris"

类群 Taxon 采样地点 Location 样本数量及采集号 Sample size and voucher no.
白桫椤 S. brunoniana 广西东兴 Dongxing, Guangxi 3: CFH09001403, CFH09001405, CFH09001406
白桫椤 S. brunoniana 海南琼中 Qiongzhong, Hainan 2: SG2100, SG2103
白桫椤 S. brunoniana 海南五指山 Wuzhishan, Hainan 6: SG2005, SG2014, SG2021, SG2030, SG2050, SG2054
白桫椤 S. brunoniana 云南河口 Hekou, Yunnan 3: CFH09000322, CFH09000324, CFH09000325
白桫椤 S. brunoniana 云南麻栗坡 Malipo, Yunnan 1: YN384
白桫椤 S. brunoniana 云南屏边 Pingbian, Yunnan 2: CFH09000301, ZXL05870
笔筒树 S. lepifera 福建福州 Fuzhou, Fujian 1: GBJ02954
笔筒树 S. lepifera 福建平潭 Pingtan, Fujian 1: GBJ04090
笔筒树 S. lepifera 台湾兰屿 Lanyu, Taiwan 2: ZXL06026, ZXL09919

Fig. 1

The nuclear genes (A) and chloroplast genes (B) phylogenetic tree of Sphaeropteris based on Bayes and Maximum likelihood method. Numbers above the branches are posterior probability (PP ≥ 0.95) from the BI analysis, and numbers under the branches are bootstrap percentages (BS ≥ 50%) of maximum likelihood analysis. The sample information is shown in Table 1."

Fig. 2

Neighbor-Net network of Sphaeropteris based on nuclear SNPs"

Fig. 3

Principal component analysis of Sphaeropteris based on SNPs. Each sample is represented by a point."

Fig. 4

The optimal K is obtained by the statistical method of ΔK"

Fig. 5

Structure of Sphaeropteris. Each sample is represented by a histogram, which is partitioned into different colors. Each color represents a genetic cluster."

Fig. 6

The significant difference analysis in leaf traits of Sphaeropteris"

Fig. 7

The spore morphology of Sphaeropteris. A, Sphaeropteris lepifera; B-D, Sphaeropteris brunoniana. B, Sample from Yunnan; C, Sample from Guangxi; D, Sample from Hainan, adopted from Wang & Dai (2010)."

Table 2

Spore morphological characteristics of Sphaeropteris"

笔筒树
S. lepifera
白桫椤 S. brunoniana
云南 Yunnan 广西 Guangxi 海南 Hainan
孢子大小 Spore size 34 μm × 46 μm 31 μm × 47 μm 35 μm × 45 μm 37 μm × 45 μm
极面观
Polar view
三角形, 三边内凹
Triangle, inset edge
三角形, 三边内凹
Triangle, inset edge
三角形, 三边直
Triangle, straight edge
三角形, 三边直
Triangle, straight edge
赤道面观
Equatorial view
扇形或近半圆形
Sector or approximate semicircle
扇形或近半圆形
Sector or approximate semicircle
扇形
Sector
扇形
Sector
表面纹
Ornamentation
短刺状
Short-echinulate
颗粒状, 细小
Granulate, small
颗粒状, 粗大
Granulate, thick
颗粒状, 细小
Granulate, small
1 Arnold ML ( 1997) Natural Hybridization and Evolution. Oxford University Press, Oxford.
2 Bunawan H, Yen CC, Yaakop S, Noor NM ( 2017) Phylogenetic inferences of Nepenthes species in Peninsular Malaysia revealed by chloroplast (trnL intron) and nuclear (ITS) DNA sequences. BMC Research Notes, 10, 67.
3 Coyne JA, Orr HA ( 2004) Speciation. Sinauer Associates, Sunderland, MA.
4 Darriba D, Taboada GL, Doallo R, Posada D ( 2012) jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772.
5 Dong SY, Zuo ZY ( 2018) On the recognition of Gymnosphaera as a distinct genus in Cyatheaceae. Annals of the Missouri Botanical Garden, 103, 1-23.
6 Evanno G, Regnaut S, Goudet J ( 2005) Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611-2620.
7 Falush D, Stephens M, Pritchard JK ( 2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
8 Guangxi Institute of Botany, Guangxi Zhuang Autonomous Region and the Chinese Academy of Sciences(2013) Flora of Guangxi,Vol. 6. Guangxi Science and Technology Publishing House,Xining. (in Chinese)
[ 广西壮族自治区中国科学院广西植物研究所( 2013) 广西植物志,第6卷. 广西科学技术出版社, 西宁.]
9 Hong DY ( 2016) Biodiversity pursuits need a scientific and operative species concept. Biodiversity Science, 24, 979-999. (in Chinese with English abstract)
[ 洪德元 ( 2016) 生物多样性事业需要科学、可操作的物种概念. 生物多样性, 24, 979-999.]
10 Johri BM ( 1984) Embryology of Angiosperms. Springer-Verlag, Berlin.
11 Klekowski EJ ( 1969) Reproductive biology of the Pteridophyta. II. Theoretical considerations. Botanical Journal of the Linnean Society, 62, 347-359.
12 Klekowski EJ, Lloyd RM ( 1968) Reproductive biology of the Pteridophyta. I. General considerations and a study of Onoclea sensibilis L. Botanical Journal of the Linnean Society, 60, 315-324.
13 Kong HZ ( 2016) Biodiversity undertakings call for extensive discussion on species concept and the criteria for species delimitation. Biodiversity Science, 24, 977-978. (in Chinese)
[ 孔宏智 ( 2016) 生物多样性事业呼唤对物种概念和物种划分标准的深度讨论. 生物多样性, 24, 977-978.]
14 Li H, Durbin R ( 2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
15 Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R ( 2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
16 Li XX, Zhou ZY, Guo SX ( 1981) The Development and Evolution of the Plant Kingdom. Science Press,Beijing. (in Chinese)
[ 李星学, 周志炎, 郭双兴 ( 1981) 植物界的发展和演化.科学出版社, 北京.]
17 Lischer HEL, Excoffier L ( 2012) PGDSpider: An automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics, 28, 298-299.
18 Liu JQ ( 2016) “The integrative species concept” and “species on the speciation way”. Biodiversity Science, 24, 1004-1008. (in Chinese with English abstract)
[ 刘建全 ( 2016) “整合物种概念”和“分化路上的物种”. 生物多样性, 24, 1004-1008.]
19 Miller MA, Pfeiffer W, Schwartz T ( 2010) Creating the CIPRES science gateway for inference of large phylogenetic trees.In: Proceedings of the Gateway Computing Environments Workshop (GCE),New Orleans.
20 Morrison DA ( 2009) Using data-display networks for exploratory data analysis in phylogenetic studies. Molecular Biology Evolution, 27, 1044-1057.
21 Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P, Pressel S, Wellman CH, Yang ZH, Schneider H, Donoghue PCJ ( 2018) The timescale of early land plant evolution. Proceedings of the National Academy of Sciences, USA, 115, 2274-2283.
22 Pritchard JK, Stephens M, Donnelly P ( 2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
23 Ranker TA, Tyron AF, Lugardon B ( 1993) Spores of the Pteridophyta: Surface, wall structure, and diversity based on electron microscope studies. Systematic Botany, 18, 377-378.
24 Rieseberg LH, Wood TE, Baack EJ ( 2006) The nature of plant species. Nature, 440, 524-527.
25 Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP ( 2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Software for Systematics and Evolution, 61, 539-542.
26 Rothfels CJ, Johnson AK, Hovenkamp PH, Swofford DL, Roskam HC, Fraser-Jenkins CR, Windham MD, Pryer KM ( 2015) Natural hybridization between genera that diverged from each other approximately 60 million years ago. The American Naturalist, 185, 433-442.
27 Soltis DE, Soltis PS ( 1987) Polyploidy and breeding systems in homosporous pteridophyta: A reevaluation. The American Naturalist, 130, 219-232.
28 Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F ( 2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS ONE, 8, e54603.
29 Stamatakis A ( 2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313.
30 Tryon RM, Tryon AF, Rudolph ED ( 1982) Ferns and allied plants with special reference to tropical America. American Fern Journal, 73(3), 94-95.
31 Wang QX, Dai XL ( 2010) Spores of Polypodiales (Filicales) from China. Science Press, Beijing. (in Chinese)
[ 王全喜, 戴锡玲 ( 2010) 中国水龙骨目(真蕨目)植物孢子形态的研究. 科学出版社, 北京.]
32 Wang QX, Yu J ( 2003) Classification of spore ornamentation in filicales under SEM. Acta Botanica Yunnanica, 25, 313-320. (in Chinese with English abstract)
[ 王全喜, 于晶 ( 2003) 扫描电镜下真蕨目孢子表面纹饰的分类. 云南植物研究, 25, 313-320.]
33 Wang WS, Mauleon R, Hu ZQ, Chebotarov D, Tai SS, Wu ZC, Li M, Zheng TQ, Fuentes RR, Zhang F, Mansueto L, Copetti D, Sanciangco M, Palis KC, Xu JL, Sun C, Fu BY, Zhang HL, Gao YM, Zhao XQ, Shen F, Cui X, Yu H, Li ZC, Chen ML, Detras J, Zhou YL, Zhang XY, Zhao Y, Kudrna D, Wang CC, Li R, Jia B, Lu JY, He XC, Dong ZT, Xu JB, Li YH, Wang M, Shi JX, Li J, Zhang DB, Lee SH, Hu WS, Poliakov A, Dubchak I, Ulat VJ, Borja FN, Mendoza JR, Ali J, Li J, Gao Q, Niu YC, Yue Z, Naredo MEB, Talag J, Wang XQ, Li JJ, Fang XD, Yin Y, Glaszmann JC, Zhang JW, Li JY, Hamilton RS, Wing RA, Ruan J, Zhang GY, Wei CC, Alexandrov N, McNally KL, Li ZK, Leung H ( 2018) Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature, 557, 43-49.
34 Wang ZJ, Guan KY ( 2011) Genetic structure and phylogeography of a relict tree fern, Sphaeropteris brunoniana (Cyatheaceae) from China and Laos inferred from cpDNA sequence variations: Implications for conservation. Journal of Systematics and Evolution, 49, 72-79.
35 Xie P ( 2016) A brief review on the historical changes in the concept of species. Biodiversity Science, 24, 1014-1019. (in Chinese with English abstract)
[ 谢平 ( 2016) 浅析物种概念的演变历史. 生物多样性, 24, 1014-1019.]
36 Yang J, Lee SH, Goddard ME, Visscher PM ( 2011) GCTA: A tool for genome-wide complex trait analysis. American Journal of Human Genetics, 88, 76-82.
37 Zhang XC, Nishida H ( 2013) Cyatheaceae. In: Flora of China,vol. 2-3(Pteridophytes) (eds Wu ZY, Raven PH, Hong DY), pp.134-138. Science Press, Beijing & Missouri Botanical Garden, St. Louis.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed