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

doi:10.17520/biods.2019111

Abstract

Abstract:

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

Guohua Zhao, Ying Wang, Hui Shang, Xile Zhou, Aihua Wang, Yufeng Li, Hui Wang, Baodong Liu, Yuehong Yan. Ancestral state reconstruction reveals the diversity and evolution of spore ornamentation in Adiantum (Pteridaceae)[J]. Biodiv Sci, 2019, 27(11): 1228-1235.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.biodiversity-science.net/EN/10.17520/biods.2019111

https://www.biodiversity-science.net/EN/Y2019/V27/I11/1228

Figures/Tables 5

References 34

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.

物种 Species	标本号及采集地 Vouchers and locality	赤道轴 × 极轴 Equatorial diam × polar diam (µm)	孢子纹饰 Spore ornamentation	图1中位置 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
扇叶铁线蕨 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
团羽铁线蕨 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
半月形铁线蕨 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
孟连铁线蕨 A. menglianense	Yan12415, Yan12409. 中国云南元江 Yuanjiang, Yunnan, China	31.5 × 26.6	颗粒 Granulate	1E
翅柄铁线蕨 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
鞭叶铁线蕨 A. caudatum	Yan12408. 中国云南元江 Yuanjiang, Yunnan, China	40.6 × 33.5	瘤状 Tuberculate	1H
白垩铁线蕨 A. gravesii	WYG393. 中国贵州贞丰 Zhenfeng, Guizhou, China	51.5 × 36.1	瘤状 Tuberculate	1I
小铁线蕨 A. mariesii	Zxl9685. 中国湖南桑植 Sangzhi, Hunan, China	36.8 × 30.1	疣状 Verrucate	1J
仙霞铁线蕨 A. juxtapositum	Yan1205071. 中国广东仁化 Renhua, Guangdong, China	60.4 × 45.7	疣状 Verrucate	1K
普通铁线蕨 A. edgewothii	Yan12412. 中国云南元江 Yuanjiang, Yunnan, China	30.0 × 25.6	瘤状 Tuberculate	1L
假鞭叶铁线蕨 A. malesianum	Yan12416, Yan12404. 中国云南元江 Yuanjiang, Yunnan, China	38.8 × 32.8	瘤状 Tuberculate	1M
梅山铁线蕨 A. × meishanianum	Yan12411. 中国云南元江 Yuanjiang, Yunnan, China	-	瘤状 Tuberculate	1N
苍山铁线蕨 A. sinicum	Yan112601, Yan12414. 中国云南元江 Yuanjiang, Yunnan, China	31.7 × 29.1	瘤状 Tuberculate	1O
哀牢山铁线蕨 A. × ailaoshanense	Yan12413, Yan12410. 中国云南元江 Yuanjiang, Yunnan, China	-	瘤状 Tuberculate	1P

物种 Species	标本号及采集地 Vouchers and locality	赤道轴 × 极轴 Equatorial diam × polar diam (µm)	孢子纹饰 Spore ornamentation	图1中位置 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
扇叶铁线蕨 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
团羽铁线蕨 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
半月形铁线蕨 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
孟连铁线蕨 A. menglianense	Yan12415, Yan12409. 中国云南元江 Yuanjiang, Yunnan, China	31.5 × 26.6	颗粒 Granulate	1E
翅柄铁线蕨 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
鞭叶铁线蕨 A. caudatum	Yan12408. 中国云南元江 Yuanjiang, Yunnan, China	40.6 × 33.5	瘤状 Tuberculate	1H
白垩铁线蕨 A. gravesii	WYG393. 中国贵州贞丰 Zhenfeng, Guizhou, China	51.5 × 36.1	瘤状 Tuberculate	1I
小铁线蕨 A. mariesii	Zxl9685. 中国湖南桑植 Sangzhi, Hunan, China	36.8 × 30.1	疣状 Verrucate	1J
仙霞铁线蕨 A. juxtapositum	Yan1205071. 中国广东仁化 Renhua, Guangdong, China	60.4 × 45.7	疣状 Verrucate	1K
普通铁线蕨 A. edgewothii	Yan12412. 中国云南元江 Yuanjiang, Yunnan, China	30.0 × 25.6	瘤状 Tuberculate	1L
假鞭叶铁线蕨 A. malesianum	Yan12416, Yan12404. 中国云南元江 Yuanjiang, Yunnan, China	38.8 × 32.8	瘤状 Tuberculate	1M
梅山铁线蕨 A. × meishanianum	Yan12411. 中国云南元江 Yuanjiang, Yunnan, China	-	瘤状 Tuberculate	1N
苍山铁线蕨 A. sinicum	Yan112601, Yan12414. 中国云南元江 Yuanjiang, Yunnan, China	31.7 × 29.1	瘤状 Tuberculate	1O
哀牢山铁线蕨 A. × ailaoshanense	Yan12413, Yan12410. 中国云南元江 Yuanjiang, Yunnan, China	-	瘤状 Tuberculate	1P

[1]	Kexin Cao, Jingwen Wang, Guo Zheng, Pengfeng Wu, Yingbin Li, Shuyan Cui. Effects of precipitation regime change and nitrogen deposition on soil nematode diversity in the grassland of northern China [J]. Biodiv Sci, 2024, 32(3): 23491-.
[2]	Qingduo Li, Dongmei Li. Analysis for the prevalence of global bat-borne Bartonella [J]. Biodiv Sci, 2023, 31(9): 23166-.
[3]	Yuanyuan Xiao, Wei Feng, Yangui Qiao, Yuqing Zhang, Shugao Qin. Effects of soil microbial community characteristics on soil multifunctionality in sand-fixation shrublands [J]. Biodiv Sci, 2023, 31(4): 22585-.
[4]	Wang Yanping, Zhang Minchu, Zhan Chengxiu. A review on the nested distribution pattern (nestedness): Analysis methods, mechanisms and conservation implications [J]. Biodiv Sci, 2023, 31(12): 23314-.
[5]	Ruiliang Zhu, Xiaoying Ma, Chang Cao, Ziyin Cao. Advances in research on bryophyte diversity in China [J]. Biodiv Sci, 2022, 30(7): 22378-.
[6]	Shumei Zhang, Wei Li, Dingnan Li. Inventory of species diversity of Liaoning higher plants [J]. Biodiv Sci, 2022, 30(6): 22038-.
[7]	Xiaoyan Jiang, Shengjie Gao, Yan Jiang, Yun Tian, Xin Jia, Tianshan Zha. Species diversity, functional diversity, and phylogenetic diversity in plant communities at different phases of vegetation restoration in the Mu Us sandy grassland [J]. Biodiv Sci, 2022, 30(5): 21387-.
[8]	Qi Zhao, Jibao Jiang, Zenglu Zhang, Qing Jin, Jiali Li, Jiangping Qiu. Species composition and phylogenetic analysis of earthworms on Hainan Island [J]. Biodiv Sci, 2022, 30(12): 22224-.
[9]	Dongmei Li, Weihong Yang, Qingduo Li, Xi Han, Xiuping Song, Hong Pan, Yun Feng. High prevalence and genetic variation of Bartonella species inhabiting the bats in southwestern Yunnan [J]. Biodiv Sci, 2021, 29(9): 1245-1255.
[10]	Ting Wang, Zengqiang Xia, Jiangping Shu, Jiao Zhang, Meina Wang, Jianbing Chen, Kanglin Wang, Jianying Xiang, Yuehong Yan. Dating whole-genome duplication reveals the evolutionary retardation of Angiopteris [J]. Biodiv Sci, 2021, 29(6): 722-734.
[11]	Qifeng Lu, Zhihuan Huang, Wenhua Luo. Characterization of complete chloroplast genome in Firmiana kwangsiensis and F. danxiaensis with extremely small populations [J]. Biodiv Sci, 2021, 29(5): 586-595.
[12]	Bo Chen, Lan Jiang, Ziyang Xie, Yangdi Li, Jiaxuan Li, Mengjia Li, Chensi Wei, Cong Xing, Jinfu Liu, Zhongsheng He. Taxonomic and phylogenetic diversity of plants in a Castanopsis kawakamiinatural forest [J]. Biodiv Sci, 2021, 29(4): 439-448.
[13]	Zhongdong Yu, Zhihe Yu, Shiyu Jin, Long Wang. Genetic diversity and toxin-producing characters of Aspergillus flavus from China [J]. Biodiv Sci, 2019, 27(8): 842-853.
[14]	Chen Zhixiang,Yao Xueying,Stephen R. Downie,Wang Qizhi. Assembling and analysis of Sanicula orthacantha chloroplast genome [J]. Biodiv Sci, 2019, 27(4): 366-372.
[15]	Xinyu Du, Jinmei Lu, Dezhu Li. Advances in the evolution of plastid genome structure in lycophytes and ferns [J]. Biodiv Sci, 2019, 27(11): 1172-1183.