Biodiversity Science ›› 2017, Vol. 25 ›› Issue (2): 136-146.doi: 10.17520/biods.2016292

• Orginal Article • Previous Article     Next Article

Phylogeography of East Asia’s Tertiary relict plants: current progress and future prospects

Yingxiong Qiu*(), Qixiang Lu, Yonghua Zhang, Yanan Cao   

  1. Key Laboratory of Conservation Biology for Endangered Wildlife of the Ministry of Education, College of Life Sciences, Zhejiang University, Hangzhou 310058
  • Received:2016-10-12 Accepted:2016-12-08 Online:2017-03-06
  • Qiu Yingxiong

In this review, based on recent studies of population genetics and phylogeographics of East Asia’s Tertiary relict plants, we have outlined the main phylogeographic patterns and processes. We also summarize common geographic and environmental factors which may contribute to the phylogeographic patterns of East Asia’s Tertiary relict plants and present future challenges and research prospects. There are four recurrent phylogeographic scenarios identified by different case studies, including: (1) the global cooling and aridification during the Middle and Late Miocene induced recent speciation, with climate change during the Late Pliocene and Pleistocene accounting for their intra-specific lineage divergence, genetic diversification and demographic expansion/contraction. The latitudinal contraction/expansion can lead to the formation of “suture zone” for some relict plants; (2) the effects of the formation of the glacial East China Sea land bridge, as a “corridor” or “filter”, have to account not only for habitat preferences per se but also for other biological features of different relict plant species; (3) the uplift of the Qinghai-Tibet Plateau (QTP) during the Late Pliocene and the intensification of East Asian monsoon system (EAMS) are the most suggestive factors responsible for the major phylogeographic break between the western and eastern lineages across the Sichuan Basin and northwestern arid regions; and (4) some Tertiary relict plants migrated southward to Taiwan from mainland China or Japan before the Pleistocene under global climatic cooling and aridification since the Late Miocene, and refugial isolation that occurred between Taiwan and mainland Asia accelerated vicariant lineage diversification and speciation. Overall, both historical and contemporary geography and environment have affected the distribution, genetic diversity, lineage divergence and speciation of East Asia’s Tertiary relict plants. Finally, we emphasize notable gaps in our knowledge due to the long-term application of simple molecular clock based on very limited genetic markers, and outline future research prospects for disentangling the evolution and biogeographic history of East Asia’s Tertiary relict flora. We present the utilization of genome data and biogeography models and integrative phylogeographic research of multi-taxon communities as possible future directions.

Key words: East Asia, Tertiary relict plants, phylogeography, glacial refugia, speciation, migration

Fig. 1

Summary of the most common genetic discontinuities (solid lines) reported by phylogeographic studies of East Asia’s Tertiary relict plants. Dashed line demarcates the boundary of Sino-Himalayan Forest sub-kingdom and Sino-Japanese Forest sub- kingdom."

1 Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary Applications, 1, 95-111.
2 An ZS, Kutzbach JE, Prell WL, Porter SC (2001) Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan Plateau since Late Miocene times. Nature, 411, 62-66.
3 Avise JC (2000) Phylogeography: the History and Formation of Species. Harvard University Press, Cambridge.
4 Axelrod DI, Al-Shehbaz I, Raven PH (1996) History of the modern flora of China. In: Floristic Characteristics and Diversity of East Asian Plants (eds Zhang AL, Wu SG), pp. 43-55. Higher Education Press, Beijing.
5 Bai WN, Wang WT, Zhang DY (2016) Phylogeographic breaks within Asian butternuts indicate the existence of a phytogeographic divide in East Asia. New Phytologist, 209, 1757-1772.
6 Canestrelli D, Bisconti R, Sacco F, Nascetti G (2014) What triggers the rising of an intraspecific biodiversity hotspot? Hints from the agile frog. Scientific Reports, 4, 5042.
7 Cao YN, Comes HP, Sakaguchi S, Chen LY, Qiu YX (2016) Evolution of East Asia’s Arcto-Tertiary relict Euptelea (Eupteleaceae) shaped by Late Neogene vicariance and Quaternary climate change. BMC Evolutionary Biology, 16, 66.
8 Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Systematic Biology, 56, 400-411.
9 Chiang TY, Schaal BA (2006) Phylogeography of plants in Taiwan and the Ryukyu Archipelago. Taxon, 55, 31-41.
10 Chen JR, Dennis WS, Fu LG, Yu YF, Harald R, Huang CJ, Zhang YT, Bruce B (1999) Cycadaceae through Fagaceae. In: Flora of China, Vol. 4. (eds Wu ZY, Raven P), Science Press, Beijing & Missouri Botanical Garden, St. Louis.
11 Chou YW, Thomas PI, Ge XJ, LePage BA, Wang CN (2011) Refugia and phylogeography of Taiwania in East Asia. Journal of Biogeography, 38, 1992-2005.
12 Crane PR, Stockey RA (1985) Growth and reproductive biology of Joffrea speirsii gen. et sp. nov., a Cercidiphyllum-like plant from the Late Paleocene of Alberta, Canada. Canadian Journal of Botany, 63, 340-364.
13 Donoghue MJ, Bell CD, Li JH (2001) Phylogenetic patterns in Northern Hemisphere plant geography. International Journal of Plant Sciences, 162, S41-S52.
14 Eyde RH (1997) Fossil record and ecology of Nyssa (Cornaceae). The Botanical Review, 63, 97-123.
15 Farjon A (2005) A Monograph of Cupressaceae and Sciadopitys. Royal Botanic Gardens, Kew.
16 Ge XJ, Hung KH, Ko YZ, Hsu TW, Gong X, Chiang TY, Chiang YC (2015) Genetic divergence and biogeographical patterns in Amentotaxus argotaenia species complex. Plant Molecular Biology Reporter, 33, 264-280.
17 Gong W, Chen C, Dobeš C, Fu CX, Koch MA (2008) Phylogeography of a living fossil: Pleistocene glaciations forced Ginkgo biloba L. (Ginkgoaceae) into two refuge areas in China with limited subsequent postglacial expansion. Molecular Phylogenetics and Evolution, 48, 1094-1105.
18 Good R (1974) The Geography of the Flowering Plants, 4th edn. Longman, London.
19 Guo WY, Yang J, Gromyko D, Ablaev AG, Wang Q, Li CS (2010) First record of Cercidiphylloxylon (Cercidiphylla- ceae) from the Palaeocene of Fushun, NE China. Journal of Systematics and Evolution, 48, 302-308.
20 Guo ZT, Sun B, Zhang ZS, Peng SZ, Xiao GQ, Ge JY, Hao QZ, Qiao YS, Liang MY, Liu JF, Yin Q, Wei J (2008) A major reorganization of Asian climate by the early Miocene. Climate of the Past, 4, 153-174.
21 Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation (Communications arising): diversity of temperate plants in East Asia. Nature, 413, 129-130.
22 Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Sciences, USA, 104, 2785-2790.
23 Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography’s past, present, and future: 10 years after. Molecular Phylogenetics and Evolution, 54, 291-301.
24 Hills LV, Klovan JE, Sweet AR (1974) Juglans eocinerea n. sp., beaufort formation (Tertiary), southwestern Banks Island, Arctic Canada. Canadian Journal of Botany, 52, 65-90.
25 Hsieh CF (2003) Composition, endemism and phytogeo- graphical affinities of the Taiwan flora. Flora of Taiwan, 6, 1-14.
26 Huang SF, Hwang SY, Wang JC, Lin TP (2004) Phylo- geography of Trochodendron aralioides (Trochoden- draceae) in Taiwan and its adjacent areas. Journal of Biogeography, 31, 1251-1259.
27 Jakob SS, Martinez-Meyer E, Blattner FR (2009) Phylogeographic analyses and paleodistribution modeling indicate Pleistocene in situ survival of Hordeum species (Poaceae) in southern Patagonia without genetic or spatial restriction. Molecular Biology and Evolution, 26, 907-923.
28 Jezkova T, Olah-Hemmings V, Riddle BR (2011) Niche shifting in response to warming climate after the last glacial maximum: inference from genetic data and niche assessments in the chisel-toothed kangaroo rat (Dipodomys microps). Global Change Biology, 17, 3486-3502.
29 Kou YX, Cheng SM, Tian S, Li B, Fan DM, Chen YJ, Soltis DE, Soltis PS, Zhang ZY (2016) The antiquity of Cyclocarya paliurus (Juglandaceae) provides new insights into the evolution of relict plants in subtropical China since the late Early Miocene. Journal of Biogeography, 43, 351-360.
30 Krassilov V (2010) Cercidiphyllum and Fossil Allies: Morphological Interpretation and General Problems of Plant Evolution and Development. Pensoft Publishers, Sofia-Moscow.
31 López-Pujol J, Zhang FM, Sun HQ, Ying TS, Ge S (2011a) Centres of plant endemism in China: places for survival or for speciation? Journal of Biogeography, 38, 1267-1280.
32 López-Pujol J, Wang HF, Zhang ZY (2011b) Conservation of Chinese plant diversity: an overview. In: Research in Biodiversity-Models and Applications (ed. Pavlinov I), pp. 163-202. InTech, Rijeka.
33 Latham RE, Ricklefs RE (1993) Continental comparisons of temperate-zone tree species diversity. In: Species Diversity in Ecological Communities (eds Ricklefs RE, Schluter D), pp. 294-314. University of Chicago Press, Chicago.
34 LePage BA, Yang H, Matsumoto M(2005) The evolution and biogeographic history of Metasequoia. In: The Geobiology and Ecology of Metasequoia (eds LePage BA, Williams CJ, Yang H), pp. 3-114. Springer, Dordrecht.
35 Li XH, Shao JW, Lu C, Zhang XP, Qiu YX (2012) Chloroplast phylogeography of a temperate tree Pteroceltis tatarinowii (Ulmaceae) in China. Journal of Systematics and Evolution, 50, 325-333.
36 Liu HY, Xing QR, Ji ZK, Xu LH, Tian YH (2003) An outline of Quaternary development of Fagus forest in China: palynological and ecological perspectives. Flora, 198, 249-259.
37 Mai DH (1995) Tertiäre Vegetationsgeschichte Mitteleuropas. Springer, Heidelberg.
38 Manchester SR (1999) Biogeographical relationships of North American Tertiary floras. Annals of the Missouri Botanical Garden, 86, 472-522.
39 Manchester SR, Chen ZD, Lu AM, Uemura K (2009) Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere. Journal of Systematics and Evolution, 47, 1-42.
40 Manns U, Wikström N, Taylor CM, Bremer B (2012) Historical biogeography of the predominantly neotropical subfamily Cinchonoideae (Rubiaceae): into or out of America? International Journal of Plant Sciences, 173, 261-286.
41 Manos PS, Stanford AM (2001) The historical biogeography of Fagaceae: tracking the Tertiary history of temperate and subtropical forests of the Northern Hemisphere. International Journal of Plant Sciences, 162, S77-S93.
42 Meng HH, Gao XY, Huang JF, Zhang ML (2015) Plant phylogeography in arid Northwest China: retrospectives and perspectives. Journal of Systematics and Evolution, 53, 33-46.
43 Meyer HW, Manchester SR (1997) Oligocene Bridge Creek Flora of the John Day Formation, Oregon. University of California Press, Berkeley.
44 Milne RI, Abbott RJ (2002) The origin and evolution of Tertiary relict floras. Advances in Botanical Research, 38, 281-314.
45 Milne RI (2006) Northern Hemisphere plant disjunctions: a window on Tertiary land bridges and climate change? Annals of Botany, 98, 465-472.
46 Nagalingum NS, Marshall CR, Quental TB, Rai HS, Little DP, Mathews S (2011) Recent synchronous radiation of a living fossil. Science, 334, 796-799.
47 Oberle B, Schaal BA (2011) Responses to historical climate change identify contemporary threats to diversity in Dodecatheon. Proceedings of the National Academy of Sciences, USA, 108, 5655-5660.
48 Onoe T (1989) Palaeoenvironmental analysis based on the Pleistocene Shiobara flora in the Shiobara volcanic basin, central Japan. Report of Geological Survey of Japan, 269, 1-207.
49 Peng YL, Hu YQ, Sun H (2003) Allozyme analysis of Davidia involucrata var. vilmoriniana and its biogeography signifi- cance. Acta Botanica Yunnanica, 25, 55-62.
(in Chinese with English abstract) [彭玉兰, 胡运乾, 孙航 (2003) 光叶珙桐的等位酶分析及其生物地理学意义. 云南植物研究, 25, 55-62.]
50 Pigg KB, Wehr WC, Ickert-Bond SM (2001) Trochodendron and Nordenskioldia (Trochodendraceae) from the Middle Eocene of Washington State, U.S.A. International Journal of Plant Sciences, 162, 1187-1198.
51 Qi XS, Chen C, Comes HP, Sakaguchi S, Liu YH, Tanaka N, Sakio H, Qiu YX (2012) Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytologist, 196, 617-630.
52 Qian H (1999) Spatial pattern of vascular plant diversity in North America north of Mexico and its floristic relationship with Eurasia. Annals of Botany, 83, 271-283.
53 Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature, 407, 180-182.
54 Qian H, Ricklefs RE (2001) Palaeovegetation (communications arising): diversity of temperate plants in east Asia. Nature, 413, 130.
55 Qiu YX, Guan BC, Fu CX, Comes HP (2009a) Did glacials and/or interglacials promote allopatric incipient speciation in East Asian temperate plants? Phylogeographic and coalescent analyses on refugial isolation and divergence in Dysosmaversipellis. Molecular Phylogenetics and Evolution, 51, 281-293.
56 Qiu YX, Qi XS, Jin XF, Tao XY, Fu CX, Naiki A, Comes HP (2009b) Population genetic structure, phylogeography, and demographic history of Platycrater arguta (Hydrangeaceae) endemic to East China and South Japan, inferred from chloroplast DNA sequence variation. Taxon, 58, 1226-1241.
57 Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552-569.
58 Sakaguchi S, Qiu YX, Liu YH, Qi XS, Kim SH, Han JY, Takeuchi Y, Worth JRP, Yamasaki M, Sakurai S (2012) Climate oscillation during the Quaternary associated with landscape heterogeneity promoted allopatric lineage divergence of a temperate tree Kalopanax septemlobus (Araliaceae) in East Asia. Molecular Ecology, 21, 3823-3838.
59 Sang T, Crawford, DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution and biogeography of Paeonia (Paeoniaceae). American Journal of Botany, 84, 1120-1136.
60 Sibuet JC, Hsu SK (2004) How was Taiwan created? Tectonophysics, 379, 159-181.
61 Su ZH, Zhang ML (2013) Evolutionary response to Quaternary climate aridification and oscillations in north-western China revealed by chloroplast phylogeography of the desert shrub Nitraria sphaerocarpa (Nitrariaceae). Biological Journal of the Linnean Society, 109, 757-770.
62 Sun YX, Moore MJ, Yue LL, Feng T, Chu HJ, Chen ST, Ji YH, Wang HC, Li JQ (2014) Chloroplast phylogeography of the East Asian Arcto-Tertiary relict Tetracentron sinense (Trochodendraceae). Journal of Biogeography, 41, 1721-1732.
63 Tanai T (1981) Geological notes on the fossil localities. In: Paleobotanical Survey to Southern Chile (ed. Nishida M), pp. 10-33. Chiba University, Chiba.
64 Tang CQ, Yang YC, Ohsawa M, Yi SR, Momohara A, Su WH, Wang HC, Zhang ZY, Peng MC, Wu ZL (2012) Evidence for the persistence of wild Ginkgo biloba (Ginkgoaceae) populations in the Dalou Mountains, southwestern China. American Journal of Botany, 99, 1408-1414.
65 Tiffney BH (1985a) The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of the Arnold Arboretum, 66, 243-273.
66 Tiffney BH (1985b) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. Journal of the Arnold Arboretum, 66, 73-94.
67 Tiffney BH, Manchester SR (2001) The use of geological and paleontological evidence in evaluating plant phylogeo- graphic hypotheses in the Northern Hemisphere Tertiary. International Journal of Plant Sciences, 162, S3-S17.
68 Uemura K (1991) Middle Miocene plant megafossil assemblages from Onnebetsu and Niupu in the Nayoro area, Hokkaido. Memoirs of the National Science Museum, Tokyo, 24, 17-26
69 Uemura K (1997) Cenozoic history of Ginkgo in East Asia. In: Ginkgo biloba—A Global Treasure: From Biology to Medicine (eds Hori T, Ridge RW, Tulecke W, del Tredici P, Trémouillaux-Guille J, Tobe, H), pp. 207-221. Springer, Tokyo.
70 Wang JF, Gong X, Chiang YC, Kuroda C (2013) Phylogenetic patterns and disjunct distribution in Ligularia hodgsonii Hook. (Asteraceae). Journal of Biogeography, 9, 1741-1754.
71 Wen J (1999) Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annual Review of Ecology and Systematics, 30, 421-455.
72 Wen J, Shi SH, Jansen R, Zimmer E (1998) Phylogeny and biogeography of Aralia sect. Aralia (Araliaceae). American Journal of Botany, 85, 866.
73 Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution, and Systematics, 36, 519-539.
74 Wolfe JA (1971) Tertiary climatic fluctuations and methods of analysis of Tertiary floras. Palaeogeography, Palaeo- climatology, Palaeoecology, 9, 27-57.
75 Wu ZY, Wang HS (1983) Phytogeography: Physical Geography in China (I). Science Press, Beijing.
(in Chinese) [吴征镒, 王荷生 (1983) 中国自然地理——植物地理(上册). 北京科学出版社, 北京.]
76 Xiang QYJ, Soltis DE (2001) Dispersal-vicariance analyses of intercontinental disjuncts: historical biogeographical implications for angiosperms in the Northern Hemisphere. International Journal of Plant Sciences, 162, S29-S39.
77 Yin HX, Yan X, Shi Y, Qian CJ, Li ZH, Zhang W, Wang LR, Li Y, Li XZ, Chen GX, Li XR, Nevo E, Ma XF (2015) The role of East Asian monsoon system in shaping population divergence and dynamics of a constructive desert shrub Reaumuria soongarica. Scientific Reports, 5, 15823.
78 Zhang YH, Wang IJ, Comes HP, Peng H, Qiu YX (2016) Contributions of historical and contemporary geographic and environmental factors to phylogeographic structure in a Tertiary relict species, Emmenopterys henryi (Rubiaceae). Scientific Reports, 6, 24041.
79 Zhao JL, Zhang L, Dayanandan S, Nagaraju S, Liu DM, Li QM (2013) Tertiary origin and Pleistocene diversification of dragon blood tree (Dracaena cambodiana-Asparagaceae) populations in the Asian tropical forests. PLoS One, 8, e60102.
[1] FAN Zi-Teng, WU Yu-Ling, WANG Xin-Ju, LI Tai-Qiang, GAO Jiang-Yun. (2019) Effects of symbiotic fungi on seed germination of interspecific hybrid progenies in Orchidaceae . Chin J Plant Ecol, 43(4): 374-382.
[2] Hu Ying, Wang Xi, Zhang Xinxin, Zhou Wei, Chen Xiaoyang, Hu Xinsheng. (2019) Advancing phylogeography with chloroplast DNA markers . Biodiv Sci, 27(2): 219-234.
[3] Morigengaowa , Hui Shang, Baodong Liu, Ming Kang, Yuehong Yan. (2019) One or more species? GBS sequencing and morphological traits evidence reveal species diversification of Sphaeropteris brunoniana in China . Biodiv Sci, 27(11): 1196-1204.
[4] Jibao Jiang, Jiangping Qiu. (2018) Origin and evolution of earthworms belonging to the family Megascolecidae in China . Biodiv Sci, 26(10): 1074-1082.
[5] Linfeng Li, Bao Liu. (2017) The roles of epigenetic variation in plant hybridization and polyploidization . Biodiv Sci, 25(6): 600-607.
[6] Yuguo Wang. (2017) Natural hybridization and speciation . Biodiv Sci, 25(6): 565-576.
[7] Chao JIANG, Ke TAN, Ming-Xun REN. (2017) Effects of monsoon on distribution patterns of tropical plants in Asia . Chin J Plan Ecolo, 41(10): 1103-1112.
[8] Jianquan Liu. (2016) “The integrative species concept” and “species on the speciation way” . Biodiv Sci, 24(9): 1004-1008.
[9] Dexing Zhang. (2016) Why is it so difficult to reach a consensus in species concept? . Biodiv Sci, 24(9): 1009-1013.
[10] Yuan Li,Jing Zhang,Ran Zhang,Puqing Song,Zhihui Zhong,Yanping Wang,Longshan Lin. (2016) Fish diversity in southwestern seas of Nansha Islands and the mouth of Beibu Bay . Biodiv Sci, 24(2): 166-174.
[11] Minyi Liang,Jianghong Ran,Siqi Liang,Yongjie Wu,Xiang Yu. (2016) Diversity and migration routes of raptors in Sichuan Province . Biodiv Sci, 24(12): 1408-1413.
[12] Zhenjie Ding,Dan Yu,Xinwei Xu. (2015) Phylogeography of Typha laxmannii in the northeast Qinghai-Tibet Plateau and adjacent areas . Biodiv Sci, 23(6): 759-766.
[13] De-Xing Zhang. (2015) Unorthodox reflections on molecular ecology research in China . Biodiv Sci, 23(5): 559-569.
[14] De-Xing Zhang. (2015) Unorthodox reflections on molecular ecology research in China . Biodiv Sci, 23(5): 559-569.
[15] Haomin Lyu,Renchao Zhou,Suhua Shi. (2015) Recent advances in the study of ecological speciation . Biodiv Sci, 23(3): 398-407.
Full text