Association between spatial genetic variation and potential distribution in tree fern Alsophila gigantea (Cyatheaceae) in Hainan Island, China

Ting WANG; Zhen  WANG; Shufeng  LI; Zhanming  YING; Xiaoxian  RUAN; Yingjuan SU

doi:10.15835/nbha49312407

Authors

Ting WANG South China Agricultural University, College of Life Sciences, Guangzhou (CN)
Zhen WANG Sun Yat-sen University, School of Life Sciences, Guangzhou (CN)
Shufeng LI Sun Yat-sen University, School of Life Sciences, Guangzhou (CN)
Zhanming YING Sun Yat-sen University, School of Life Sciences, Guangzhou; Xiangtan University, College of Chemistry, Xiangtan (CN)
Xiaoxian RUAN un Yat-sen University, School of Life Sciences, Guangzhou (CN)
Yingjuan SU Sun Yat-sen University, School of Life Sciences, Guangzhou; Research Institute of Sun Yat-sen University in Shenzhen, Shenzhen (CN)

DOI:

https://doi.org/10.15835/nbha49312407

Keywords:

Alsophila gigantea, environmental factors, genetic diversity, Hainan Island, ISSR, potential distribution, spatial genetic structure, tree ferns

Abstract

Spatial genetic variation involves spatial genetic structure (SGS) and genetic diversity is important genetic features of plants. We first evaluated spatial genetic structure (SGS) and genetic diversity among four populations of Alsophila gigantea from Hainan Island, China, using inter-simple sequence repeat (ISSR) markers. Significant but weak FSGS was found in A. gigantea. High genetic diversity was identified at the species level and the population level. AMOVA analysis revealed a low level of genetic differentiation among the four populations with high gene flow. Mantel test showed no significant correlation between genetic distance and geographic distance. It was found that association between annual mean temperature and annual precipitation with FSGS. Combined with these spatial genetic variation, abundant precipitation and suitable temperature create a stable environment for A. gigantea in Hainan Island, which allows the fern to expand rapidly during the LGM. These results further emphasized the role of outcrossing, and history and environmental factors in the evolution of A. gigantea. This study also provided new insights on in local adaptation of A. gigantea to environmental fluctuations, and available genetic data to enhance the conservation for relict tree ferns.

References

Au GH (2004). Research advance in the Cyatheaceae. Journal of Neijiang Teachers College 19:79-82. http://en.cnki.com.cn/Article_en/CJFDTOTAL-NJSG200406018.htm

Bucharova A, Munzbergova Z (2012). Gene flow among populations of two rare co-occurring fern species differing in ploidy level. PLoS One 7(9):e45855. https://doi.org/10.1371/journal.pone.0045855

Chen ML (1995). The study of genetic structure of Sphaeropteris lepifera (HooK.) Tryon (Cyatheaceae) in Taiwan. M.S. thesis, Department of Biology, Natl. Taiwan Normal University.

Chiou WL, Huang YM, Lee PH (2003). Mating systems of Cyatheaceae native to Taiwan. In: Chandra S, Srivastava M (Eds). Pteridology in the new millennium. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-2811-9_32

Chiou WL, Lee PH, Ying SS (2000). Reproductive biology of gametophytes of Cyathea podophylla (Hook.) Copel. Taiwan Journal of Forest Science 15:1-12. https://doi.org/10.7075/TJFS.200003.0001

Chung MY, Chung MG (2013). Significant spatial aggregation and fine-scale genetic structure in the homosporous fern Cyrtomium falcatum (Dryopteridaceae). New Phytologist 199:663-672. https://doi.org/10.1111/nph.12293

CITES (2017). Convention on international trade in endangered species of wild fauna and flora. Appendices I, II, and III. Retrieved 2018 June 7 from https://cites.org/eng/app/appendices.php.

Dyer AF (1994). Natural soil spore banks – can they be used to retrieve lost ferns? Biodiversity and Conservation 3:160-175. https://doi.org/10.1007/BF02291886

Frankham R (1997). Do island populations have less genetic variation than mainland populations? Heredity 78:311-327. https://doi.org/10.1038/hdy.1997.46

Fu LG (1992). Red List of China – rare and endangered plants. Vol. 1 (Science Press: Beijing).

Hope G (2005). The quaternary in Southeast Asia. In: Gupta A (Ed). The Physical Geography of Southeast Asia. Oxford University Press, Oxford, UK, pp 24-37. https://doi.org/10.1093/oso/9780199248025.003.0012

Huang R, Chu QH, Lu GH, Wang YQ (2019). Comparative studies on population genetic structure of two closely related selfing and outcrossing Zingiber species in Hainan Island. Scientific Reports 9:17997. https://doi.org/10.1038/s41598-019-54526-y

Jimenez A, Holderegger R, Csencsics D, Quintanilla LG (2010). Microsatellites reveal substantial among-population genetic differentiation and strong inbreeding in the relict fern Dryopteris aemula. Annals of Botany 106:149-155. https://doi.org/10.1093/aob/mcq094

Johns RJ, Edwards PJ (1991). Vegetative reproduction in Pteridophytes. Curtis's Botanical Magazine 8:107-158. https://doi.org/10.1111/j.1467-8748.1991.tb00370.x

Knobloch IW (1969). The spore pattern in some species of Cheilanthes. American Journal of Botany 56:646-653. https://doi.org/10.1002/j.1537-2197.1969.tb07581.x

Kolbe JJ, Glor RE, Rodriguez-Schettino L, Chamizo-Lara A, Larson A, Losos JB (2004). Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177-181. https://doi.org/10.1038/nature02807

Lehnert M (2011). Species of Cyathea in America related to the western Pacific species C. decurrens. Phytotaxa 26:39-59. https://doi.org/10.11646/phytotaxa.26.1.6

Lehnert SJ, Dibacco C, Van-Wyngaarden M, Jeffery NW, Ben-Lowen J, Sylvester EVA, … Bradbury IR (2019). Fine-scale temperature-associated genetic structure between inshore and offshore populations of sea scallop (Placopecten magellanicus). Heredity 122:69-80. https://doi.org/10.11646/phytotaxa.26.1.6

Li J, Haufler CH (1999). Genetic variation, breeding systems, and patterns of diversification in Hawaiian Polypodium (Polypodiaceae). Systematic Botany 24:339-355. https://doi.org/10.2307/2419694

Li Y, Wei C, He XY, Chen W, Xu S (2019). Prediction of suitable habitat for lycophytes and ferns in northeast China: A case study on Athyrium brevifrons. Chinese Geographical Science 29(6):1011-1023. https://doi.org/10.1007/s11769-019-1085-4

Li Y, Zhang YL, Jiang CD, Wang T, Wang Q, Shi L (2010). Effect of storage temperature on spore viability and early gametophyte development of three vulnerable species of Alsophila (Cyatheaceae). Australian Journal of Botany 58: 89-96. https://doi.org/10.1071/BT09180

Liu YX, Pham HT, He ZQ, Wei C (2020). Phylogeography of the cicada Platypleura hilpa in subtropical and tropical East Asia based on mitochondrial and nuclear genes and microsatellite markers. International Journal of Biological Macromolecules 151:529-544. https://doi.org/10.1016/j.ijbiomac.2020.02.183

Loveless MD, Hamrick JL (1984). Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics 15:65-95. https://doi.org/10.1146/annurev.es.15.110184.000433

Makgomol K (2006). Morphology of fern spores from Phu Phan National Park. Kasetsart Journal (Natural Science) 40:116-122. https://doi.org/10.1146/annurev.es.15.110184.000433

Manel S, Williams HC, Ormerod SJ (2001). Evaluating presence-absence models in ecology: the need to account for prevalence. Journal of Applied Ecology 38(5):921-931. https://doi.org/10.1046/j.1365-2664.2001.00647.x

Mcveigh I (1937). Vegetative reproduction of the fern sporophyte. Botanical Review 3:457-497. https://doi.org/10.1007/BF02870311

Mehltreter K, García-Franco JG (2008). Leaf phenology and trunk growth of the deciduous tree fern Alsophila firma (Baker) D.S. Conant in a lower montane Mexican forest. American Fern Journal 98:1-13. https://doi.org/10.1640/0002-8444(2008)98[1:LPATGO]2.0.CO;2

Mo Y, Shi Y (1987). Paleomagnetic study and tectonic evolution of Hainan terrane and its vicinal continental coast the late Mesozoic to Cenozoic. Journal of Nanjing University 23:521-532. http://en.cnki.com.cn/Article_en/CJFDTOTAL-NJDZ198703013.htm

Nielsen LR (2004). Molecular differentiation within and among island populations of the endemic plant Scalesia affinis (Asteraceae) from the Galápagos Islands. Heredity 93:434-442. https://doi.org/10.1038/sj.hdy.6800520

Paul A, Bhattacharjee S, Choudhury BI, Khan ML (2015). Population structure and regeneration status of Cyathea gigantea (Wallich ex Hook. f.) Holttum, a tree fern in Arunachal Pradesh, India. Journal of Forest and Environmental Science 31:164-176. https://doi.org/10.7747/JFES.2015.31.3.164

Peck JH, Peck CJ, Farrar DR (1990). Influences of life history attributes on formation of local and distant fern populations. American Fern Journal 80:126-142. https://doi.org/10.2307/1547200

Pryor KV, Young JE, Rumsey FJ, Edwards KJ, Bruford MW, Rogers HJ (2001). Diversity, genetic structure and evidence of outcrossing in British populations of the rock fern Adiantum capillus-veneris using microsatellites. Molecular Ecology 10:1881-1894. https://doi.org/10.1046/j.1365-294X.2001.01343.x

Ramírez-Barahona S, Eguiarte LE (2014). Changes in the distribution of cloud forests during the last glacial predict the patterns of genetic diversity and demographic history of the tree fern Alsophila firma (Cyatheaceae). Journal of Biogeography 41:2396-2407. https://doi.org/10.1111/jbi.12396

Ramírez-Barahona S, Eguiarte LE (2015). Spatial genetic analyses reveal strong genetic structure in two populations of the outcrossing tree fern Alsophila firma (Cyatheaceae). Botanical Journal of the Linnean Society 177:439-449. https://doi.org/10.1111/boj.12248

Saro I, Garcia-Verdugo C, Gonzalez-Perez MA, Naranjo A, Santana A, Sosa PA (2019). Genetic structure of the Canarian palm tree (Phoenix canariensis) at the island scale: does the ‘island within islands’ concept apply to species with high colonisation ability? Plant Biology 21:101-109. https://doi.org/10.1111/plb.12913

Shi YF, Cui ZJ, Su Z (2006). The quaternary glaciations and environmental variations in China. Shijiazhuang: Hebei Science and Technology Press.

Su YJ, Wang T, Deng F (2010). Contrasting genetic variation and differentiation on Hainan Island and the Chinese mainland populations of Dacrycarpus imbricatus (Podocarpaceae). Biochemical Systematics and Ecology 38:576-584. https://doi.org/10.1016/j.bse.2010.07.003

Su YJ, Wang T, Deng F (2010). Population genetic variation, differentiation and bottlenecks of Dacrydium pectinatum (Podocarpaceae) in Hainan Island, China: implications for its conservation. Australian Journal of Botany 58:318-326. https://doi.org/10.1071/BT09106

Torres E, Riofrio ML, Iriondo JM (2019). Complex fine-scale spatial genetic structure in Epidendrum rhopalostele: an epiphytic orchid. Heredity 122:458-467. https://doi.org/10.1038/s41437-018-0139-1

Tryon R (1970). Development and evolution of fern floras of oceanic islands. Biotropica 2:76-84. https://doi.org/10.2307/2989765

Tryon R (1972). Endemic areas and geographic speciation in tropical American ferns. Biotropica 4:121-131. https://doi.org/10.2307/2989774

Wang T, Hong YF, Wang Z, Su YJ (2019). Characterization of the complete chloroplast genome of Alsophila gigantea (Cyatheaceae), an ornamental and CITES giant tree fern. Mitochondrial DNA Part B Resources 4(1):967-968. https://doi.org/10.1080/23802359.2019.1580162

Wang T, Su YJ, Li XY, Zhen B, Chen GP, Wang BS (2003). RAPD analysis of the genetic variation within populations of a relict tree fern, Alsophila spinulosa (Cyatheaceae). Acta Ecologica Sinica 23:1200-1206. https://doi.org/10.1023/A:1022289509702

Wang T, Su YJ, Li Y (2012). Population genetic variation in the tree fern Alsophila spinulosa (Cyatheaceae): effects of Reproductive strategy. PLoS One 7(7):e41780. https://doi.org/10.1371/journal.pone.0041780

Wang XM, Zheng X, Wu H, Zhou XJ, Kuang HH, Guo HL, … Li W (2016). Multilocus sequence typing of clinical isolates of Burkholderia pseudomallei collected in Hainan, a tropical island of Southern China. American Journal of Tropical Medicine and Hygiene 95(4):760-764. https://doi.org/10.4269/ajtmh.16-0280

Wang XX, Long WX, Yang XB, Xiong MH, Kang Y, Huang J, … Li SX (2016). Patterns of plant diversity within and among three tropical cloud forest communities in Hainan Island. Acta Phytoecologica Sinica 40(05):469-479. https://doi.org/10.17521/cjpe.2016.0021

White RA (1969). Vegetative reproduction in the ferns II root buds in Amphora denium. Bulletin of the Torrey Botanical Club 96:10-19. https://doi.org/10.2307/2484004

Yan JA (2006). Paleontology and ecologic environmental evolution of the Quaternary in Hainan Island. Journal of Palaeogeography 8:103-115. https://doi.org/10.1360/aps040120

Zhang JJ, Jiang F, Li GY, Qin W, Wu T, Xu F, Hou YS, Song PF, Cai ZY, Zhang TZ (2021). The four antelope species on the Qinghai-Tibet plateau face habitat loss and redistribution to higher latitudes under climate change. Ecological Indicators 123:107337. https://doi.org/10.1016/j.ecolind.2021.107337

Zhang XC, Nishida H (2013). Cyatheaceae. In: Wu ZY, Raven PH, Hong DY (Eds). Flora of China. Vol. 2–3 (Pteridophytes). Beijing: Science Press, pp 134-138. http://www.iplant.cn/foc

Zhang Z, Liu R (1989). The stage-division of quaternary volcanic rocks in Hainan Island. Chinese Journal of Geology 1:67-76. http://en.dzkx.org/article/id/geology_10352

Zhang Z, Stephan WG, Li JH, Fischer GA, Ren MX, Song XQ (2019). Pollen-mediated gene flow ensures connectivity among spatially discrete subpopulations of Phalaenopsis pulcherrima, a tropical food-deceptive orchid. BMC Plant Biology 19:597. https://doi.org/10.1186/s12870-019-2179-y