Biodiversity Science ›› 2019, Vol. 27 ›› Issue (11): 1228-1235.doi: 10.17520/biods.2019111

• Original Papers • Previous Article     Next Article

Ancestral state reconstruction reveals the diversity and evolution of spore ornamentation in Adiantum (Pteridaceae)

Guohua Zhao1, 2, Ying Wang2, Hui Shang2, Xile Zhou3, Aihua Wang4, Yufeng Li5, Hui Wang1, Baodong Liu6, Yuehong Yan2, *()   

  1. 1 Fairylake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen, Guangdong 518004;
    2 Shanghai Chenshan Botanical Garden, Shanghai Chenshan Plant Science Research Center, Chinese Academy of Sciences, Shanghai 201602
    3 Xiangxi Tujia and Miao Autonomous Prefecture Forest Resources Monitoring Center, Jishou, Hunan 416000
    4 Key Laboratory of Beibu Gulf Environment Change and Resources Use of Ministry of Education, Nanning Normal University, Nanning 530001
    5 School of Life Science, Hunan University of Science and Technology, Xiangtan, Hunan 411201
    6 Harbin Normal University, Key Laboratory of Plant Biology, College of Heilongjiang Province, Harbin 150025
  • Received:2019-03-29 Accepted:2019-10-08 Online:2020-01-17
  • Yan Yuehong

Spore morphology is diverse and complex in ferns, thus serving as an important indicator of taxonomy. In conjunction, morphological traits and phylogeny are used to study taxonomy and recent character evolution. This study analyzes the evolution of spore ornamentation in once-pinnate maidenhair ferns (Adiantum) using scanning electron microscopy and ancestral state reconstruction. Our results show that there are five ornamental types in once-pinnate maidenhair ferns: psilate, scabrate, granulate, verrucate and tuberculate. The ancestral state of spore ornamentation in Adiantum is probably tuberculate, with verrucate ornamentation possibly deriving from tuberculate. We suggest that spore ornamentation evolved from simple to complex in Adiantum. In other words, the more evolutionary species, will with a more complex spore ornamentation.

Key words: fern, spore ornamentation, phylogenetic, character evolution

Table 1

The locality information and spore morphology in Adiantum"

Vouchers and locality
赤道轴 × 极轴
Equatorial diam ×
polar diam (µm)
Spore ornamentation
Position in Fig. 1
A. latifolium Zxl9882. 泰国曼谷植物标本馆 Bangkok Herbarium, Bangkok, Thailand 33.5 × 27.0 粗糙 Scabrate 1A
A. flabellulatum
Zxl10018. 中国广东南岭国家森林公园 Nanling National Forest Park, Guangdong, China 45.5 × 31.2 颗粒 Granulate 1B
A. capillus-junonis
Zxl9959. 中国广东南岭国家森林公园 Nanling National Forest Park, Guangdong, China 46.5 × 43.0 光滑 Psilate 1C
A. philippense
Yan12405, Yan12086. 中国云南元江; Zxl9839. 泰国彭世洛府屯萨朗峦国家公园
Yan12405, Yan12086. Yuanjiang, Yunnan, China; Zxl9839. Thung Salaeng Luang National Park, Phitsanulok, Thailand
33.4 × 25.7 粗糙 Scabrate 1D
A. menglianense
Yan12415, Yan12409. 中国云南元江 Yuanjiang, Yunnan, China 31.5 × 26.6 颗粒 Granulate 1E
A. soboliferum
Yan11393. 中国海南昌江 Changjiang, Hainan, China 34.0 × 30.5 颗粒 Granulate 1F
A. zollingeri Zxl9812, Zxl9911, ZXL9851. 泰国碧武里府康卡沾国家公园
Kaeng Krachan National Park, Phetchaburi, Thailand
34.0 × 27.3 瘤状 Tuberculate 1G
A. caudatum
Yan12408. 中国云南元江 Yuanjiang, Yunnan, China 40.6 × 33.5 瘤状 Tuberculate 1H
A. gravesii
WYG393. 中国贵州贞丰 Zhenfeng, Guizhou, China 51.5 × 36.1 瘤状 Tuberculate 1I
A. mariesii
Zxl9685. 中国湖南桑植 Sangzhi, Hunan, China 36.8 × 30.1 疣状 Verrucate 1J
A. juxtapositum
Yan1205071. 中国广东仁化 Renhua, Guangdong, China 60.4 × 45.7 疣状 Verrucate 1K
A. edgewothii
Yan12412. 中国云南元江 Yuanjiang, Yunnan, China 30.0 × 25.6 瘤状 Tuberculate 1L
A. malesianum
Yan12416, Yan12404. 中国云南元江 Yuanjiang, Yunnan, China 38.8 × 32.8 瘤状 Tuberculate 1M
A. × meishanianum
Yan12411. 中国云南元江 Yuanjiang, Yunnan, China - 瘤状 Tuberculate 1N
A. sinicum
Yan112601, Yan12414. 中国云南元江 Yuanjiang, Yunnan, China 31.7 × 29.1 瘤状 Tuberculate 1O
A. × ailaoshanense
Yan12413, Yan12410. 中国云南元江 Yuanjiang, Yunnan, China - 瘤状 Tuberculate 1P

Fig. 1

Spore morphology in once-pinnate maidenhair ferns (Adiantum). (A) A. latifolium; (B) A. flabellulatum; (C) A. capillus-junonis; (D) A. philippense; (E) A. menglianense; (F) A. soboliferum; (G) A. zollingeri; (H) A. caudatum; (I) A. gravesii; (J) A. mariesii; (K) A. juxtapositum; (L) A. edgewothii; (M) A. malesianum; (N) A. × meishanianum; (O) A. sinicum; (P) A. × ailaoshanense."

Fig. 2

Spore size of Adiantum. Yellow shapes indicate A. Ser. Gravesiana. Blue shapes indicate A. Ser. Caudata. Black shapes indicate outgroup."

Fig. 3

The phylogenetic tree constructed based on five chloroplast markers (rbcL, atpB, atpA, trnL-F, rps4-trnS). Numbers on branches are support values (ML/MP/BI). *, ML, MP = 100%, and BI = 1.0."

Fig. 4

Evolution of spore ornamentation in once-pinnate maidenhair ferns (Adiantum)"

1 Barrington DS, Paris CA, Ranker TA ( 1986) Systematic inferences from spore and stomate size in the ferns. American Fern Journal, 76, 149-159.
2 Blackmore S, Barnes SH ( 1987) Embryophyte spore walls: Origin, development, and homologies. Cladistics, 3, 185-195.
3 Campo MV, Lugardon B ( 1973) Structure grenue infratectale de l’ectexine des pollens de quelques Gymnospermes et Angiospermes. Pollen et Spores, 15, 171-189. (in French)
4 Caroline PD, Patrica LF ( 2001) Modern pollen precipitation from an elevational transect in central Jordan and its relationship to vegetation. Journal of Biogeography, 28, 1195-1210.
5 Co-David D, Langeveld D, Noordeloos ME ( 2009) Molecular phylogeny and spore evolution of Entolomataceae. Persoonia, 23, 147.
6 Devi S ( 1979) Spore types, morphological evolution and phylogeny in the Pteridaceae. Grana, 18, 41-46.
7 Hummel J, Gee CT, Südekum KH, Sander PM, Clauss M ( 2008) In vitro digestibility of fern and gymnosperm foliage: Implications for sauropod feeding ecology and diet selection. Proceedings of the Royal Society B: Biological Sciences, 275, 1015-1021.
8 Lellinger DB ( translated by Xiang JY, Wu SG ) ( 2007) A Modern English-Chinese Glossary for Taxonomic Pteridology. Yunnan Science and Technology Press, Kunming. (in Chinese)
[ 向建英, 武素功译 ( 2007) 现代英中对照蕨类植物分类学词汇. 云南科技出版社, 昆明.]
9 Liu HM, Zhang XC, Chen ZD, Qiu YL ( 2007) Inclusion of the Eastern Asia endemic genus Sorolepidium in Polystichum (Dryopteridaceae) evidence from the chloroplast rbcL gene and morphological characteristics. Chinese Science Bulletin, 52, 631-638.
10 Lu JM, Wen J, Lutz S, Wang YP, Li DZ ( 2012) Phylogenetic relationships of Chinese Adiantum based on five plastid markers. Journal of Plant Research, 125, 237-249.
11 Luo YL, Sun XJ ( 2001) Vegetation evolution in the northen South China Sea region since 40 ka BP—An attempt to reconstruct palaeovegetation based on biomization. Acta Botanica Sinica, 43, 1202-1206.
12 Mehltreter K, Mehltreter K, Walker L, Sharpe J ( 2010) Fern Ecology. Cambridge University Press, Cambridge.
13 Midgley J, Midgley G, Bond W ( 2002) Why were dinosaurs so large? A food quality hypothesis. Evolutionary Ecology Research, 4, 1093-1095.
14 Ottosson JG, Anderson JM ( 1983) Number, seasonality and feeding habits of insects attacking ferns in Britain: An ecological consideration. Journal of Animal Ecology, 52, 385-406.
15 Patricia L ( 1992) Spatial patterns of atmospheric pollen dispersal in the Colorado Rocky Mountains, USA. Review of Palaeobotany and Palynology, 74, 293-313.
16 The Chromosome Counts Database ( CCDB) ( 2014) A community resource of plant chromosome numbers. 2014) A community resource of plant chromosome numbers. .
17 Shang H, Yan YH ( 2014) Soral crypsis of insect larvea on bracken ferns. Chinese Journal of Nature, 36, 426-430. (in Chinese with English abstract)
[ 商辉, 严岳鸿 ( 2014) 昆虫幼虫对凤尾蕨属植物孢子囊群的拟态. 自然杂志, 36, 426-430.]
18 Shang H, Wang Y, Zhu XF, Zhao GH, Wang FG, Lu JM ( 2016) Likely allopatric origins of Adiantum × meishanianum (Pteridaceae) through multiple hybridizations. Journal of Systematics and Evolution, 54, 528-534.
19 Smart J, Hughes NF ( 1973) The Insect and the Plant: Progressive Palaeoecological Integration. John Wiley & Sons, New York.
20 Tanaka N, Uehara K, Murata J ( 2004) Correlation between pollen morphology and pollination mechanisms in the Hydrocharitaceae. Journal of Plant Research, 117, 265-276.
21 Tao ZB, Wortley AH, Lu L, Li DZ, Wang H, Blackmore S ( 2018) Evolution of angiosperm pollen. 6. The Celastrales, Oxalidales, and Malpighiales (Com) clade and Zygophyllales. Annals of the Missouri Botanical Garden, 103, 393-442.
22 Tryon AF ( 1985) Spores of myrmecophytic ferns. Proceedings of the Royal Society of Edinburgh, Section B: Biological Sciences, 86, 105-110.
23 Tryon AF, Lugardon B ( 1991) Spores of the Pteridophyta: Surface, Wall Structure, and Diversity Based on Electron Microscope Studies. Springer Verlag, New York.
24 Walker JW ( 1974) Evolution of exine structure in the pollen of primitive angiosperms. American Journal of Botany, 61, 891-902.
25 Walker TG ( 1985) Spore filaments in the ant-fern Lecanopteris mirabilis—An alternative viewpoint. Proceedings of the Royal Society of Edinburgh Section B: Biological Sciences, 86, 111-114.
26 Wang AH, Sun Y, Wang FG, Schneider H, Zhai JW, Liu DM, Zhou JS, Xing FW, Chen HF ( 2015 a) Identification of the relationship between Chinese Adiantum reniforme var. sinense and Canary Adiantum reniforme. BMC Plant Biology, 15, 36.
27 Wang FG, Liu HM, He CM, Yang DM, Xing FW ( 2015 b) Taxonomic and evolutionary implication of spore ornamentation in Davalliaceae. Journal of Systematics and Evolution, 53, 72-81.
28 Wang QX, Dai XL ( 2001) Spores of Polypodiales (Filicales) from China. Science Press, Beijing. (in Chinese)
[ 王全喜, 戴锡玲 ( 2001) 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.]
29 Wang WM ( 2009) Progress and prospect of studies on palynology in China. Acta Palaeontologica Sinica, 48, 338-346. (in Chinese with English abstract)
[ 王伟铭 ( 2009) 中国孢粉学的研究进展与展望. 古生物学报, 48, 338-346.]
30 Wang Y, Shang H, Gu YF, Wei HJ, Zhao GH, Dai XL, Yan YH ( 2015) A new cryptic hybrid species of Adiantum L. (Pteridaceae) indentified by nuclear and chloroplast DNA sequences. Chinese Science Bulletin, 60, 922-932. (in Chinese with English abstract)
[ 王莹, 商辉, 顾钰峰, 韦宏金, 赵国华, 戴锡玲, 严岳鸿 ( 2015) 用核DNA和叶绿体DNA序列鉴别铁线蕨属Adiantum L. (凤尾蕨科)新的隐性杂交种. 科学通报, 10, 922-932.]
31 Wang Y, Shang H, Zhou XL, Zhao GH, Dai XL, Yan YH ( 2015 c) Adiantum × ailaoshanense (Pteridaceae), a new natural hybrid from Yunnan, China. Phytotaxa, 236, 266-272.
32 Wei R, Schneider H, Zhang XC ( 2013) Toward a new circumscription of the twinsorus-fern genus Diplazium (Athyriaceae): A molecular phylogeny with morphological implications and infrageneric taxonomy. Taxon, 62, 441-457.
33 Yang ZJ, Xu JM ( 2002) Advances in studies on relationship among pollen, vegetation and climate. Acta Phytoecologica Sinica, 26(Suppl.), 73-81. (in Chinese with English abstract)
[ 杨振京, 徐建明 ( 2002) 孢粉-植被-气候关系研究进展. 植物生态学报, 26(增刊), 73-81.]
34 Zhang WY, Kuo LY, Li FW, Wang CN, Chiou WL ( 2014) The hybrid origin of Adiantum meishanianum (Pteridaceae): A rare and endemic species in Taiwan. Systematic Botany, 39, 1034-1041.
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