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Genetic divergence within the monotypic tree genus Platycarya (Juglandaceae) and its implications for species’ past dynamics in subtropical China

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Abstract

Subtropical East Asia harbours a large plant diversity that is often attributed to allopatric speciation in this topographically complex region characterized by a relative climate stability. Here, we use observations of Platycarya, a widespread subtropical Asian tree genus, to explore the consequences of past climate stability on species’ evolutionary history in subtropical China. This genus has a controversial taxonomy: while it is now prevailingly treated as monotypic, two species have been originally described, Platycarya strobilacea and P. longipes. Previous information from species distribution models, fossil pollen data and genetic data based on chloroplast DNA (cpDNA) were integrated with newly obtained genetic data from the two putative species. We used both cpDNA (psbA-trnH and trnL-F intergenic spacers, including a partial trnL gene sequence) and nuclear markers. The latter included sequences of the internal transcribed spacer region (ITS1–5.8S–ITS2) of the nuclear ribosomal DNA and random genomic single nucleotide polymorphisms. Using these nuclear genetic markers, we found interspecific genetic divergence fitting with the ‘two species’ scenario and geographically structured intraspecific variation. Using cpDNA markers, we also found geographically structured intraspecific variation. Despite deep inter- and intraspecific genetic divergence, we detected genetic admixture in southwest China. Overall, our findings of genetic divergence within Platycarya support the hypothesis of allopatric speciation. However, episodes of population interconnection were identified, at least in southwest China, suggesting that the genus has had a dynamic population history.

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References

  • Atkinson PJ, Upson T (2006) Platycarya strobilacea. Curtis’s Bot Mag 23:77–83

    Article  Google Scholar 

  • Bai WN, Wang WT, Zhang DY (2014) Contrasts between the phylogeographic patterns of chloroplast and nuclear DNA highlight a role for pollen-mediated gene flow in preventing population divergence in an East Asian temperate tree. Mol Phylogenet Evol 81:37–48

    Article  PubMed  Google Scholar 

  • Barthlott W, Mutke J, Rafiqpoor D, Kier G, Kreft H (2005) Global centers of vascular plant diversity. Nova Acta Leopold 92:61–83

    Google Scholar 

  • Brumfield RT, Beerli P, Nickerson DA, Edwards SV (2003) The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol Evol 18:249–256

    Article  Google Scholar 

  • 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 Evol Biol 16:66

    Article  PubMed  PubMed Central  Google Scholar 

  • Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen S-C, Zhang L, Zeng J, Shi F, Yang H, Mao Y-R, Fu C-X (2012) Geographic variation of chloroplast DNA in Platycarya strobilacea (Juglandaceae). J Syst Evol 50:374–385

    Article  Google Scholar 

  • China Plant B O L Group, Li D-Z, Gao L-M, Li H-T, Wang H, Ge X-J, Liu J-Q, Chen Z-D, Zhou S-L, Chen S-L, Yang J-B, Fu C-X, Zeng C-X, Yan H-F, Zhu Y-J, Sun Y-S, Chen S-Y, Zhao L, Wang K, Yang T, Duan G-W (2011) Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proc Natl Acad Sci U S A 108:19641–19646

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  CAS  PubMed  Google Scholar 

  • Comes HP, Abbott RJ (2001) Molecular phylogeography, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution 55:1943–1962

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small amounts of fresh leaf tissue. Phytochem Bull 19:11–15. doi:10.2307/4119796

    Google Scholar 

  • Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious v5.1. Available at: http://www.geneious.com

  • Du FK, Petit RJ, Liu JQ (2009) More introgression with less gene flow: chloroplast vs. mitochondrial DNA in the Picea asperata complex in China, and comparison with other conifers. Mol Ecol 18:1396–1407

    Article  CAS  PubMed  Google Scholar 

  • Duminil J, Caron H, Scotti I, Cazal SO, Petit RJ (2006) Blind population genetics survey of tropical rainforest trees. Mol Ecol 15:3505–3513

    Article  CAS  PubMed  Google Scholar 

  • Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci U S A 107:16196–16200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Wang Z, Tang Z (2011) Atlas of woody plants in China: distribution and climate. High Education Press, Beijing

    Book  Google Scholar 

  • Feng G, Mao L, Sandel B, Swenson NG, Svenning J-C (2016) High plant endemism in China is partially linked to reduced glacial-interglacial climate change. J Biogeogr 43:145–154

    Article  Google Scholar 

  • Fukuhara T, Tokumaru S (2014) Inflorescence dimorphism, heterodichogamy and thrips pollination in Platycarya strobilacea (Juglandaceae). Ann Bot 113:467–476

    Article  PubMed  Google Scholar 

  • Guichoux E, Garnier-Gere P, Lagache L, Lang T, Boury C, Petit RJ (2013) Outlier loci highlight the direction of introgression in oaks. Mol Ecol 22:450–462

    Article  CAS  PubMed  Google Scholar 

  • Harrison RG, Bogdanowicz SM (1997) Patterns of variation and linkage disequilibrium in a field cricket hybrid zone. Evolution 51:493–505

    Article  CAS  PubMed  Google Scholar 

  • Harrison SP, Yu G, Takahara H, Prentice IC (2001) Palaeovegetation-diversity of temperate plants in east Asia. Nature 413:129–130

    Article  CAS  PubMed  Google Scholar 

  • Hartigan JA, Hartigan PM (1985) The dip test of unimodality. Ann Stat 13:70–84

    Article  Google Scholar 

  • Kou Y, Cheng S, Tian S, Li B, Fan D, Chen Y, Soltis DE, Soltis PS, Zhang Z (2016) The antiquity of Cyclocarya paliurus (Juglandaceae) provides new insights into the evolution of relict plants in subtropical China since the late Early Miocene. J Biogeogr 43:351–360

    Article  Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS One 2:e508

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuang KZ, Cheng SH, Li PC, Lu AM (1979) Juglandaceae. In: Flora reipublicae popularis sinicae. Science Press, Beijing, pp 8–42

  • Le Bras Y, Roult A, Monjeaud C, Bahin M, Quenez O, Heriveau C, Bretaudeau A, Sallou O, Collin O (2013) Towards a life sciences virtual research environment: an e-science initiative in western France. Conference: JOBIM, New York City

  • López-Pujol J, Zhang F-M, Sun H-Q, Ying T-S, Ge S (2011) Centres of plant endemism in China: places for survival or for speciation? J Biogeogr 38:1267–1280

    Article  Google Scholar 

  • Li J, Zheng Z, Huang K, Yang S, Chase B, Valsecchi V, Carré M, Cheddadi R (2013) Vegetation changes during the past 40,000 years in central China from a long fossil record. Quat Int 310:221–226

    Article  Google Scholar 

  • Li R-Q, Chen Z-D, Lu A-M (2005) Organogenesis of the inflorescence and flowers in Platycarya strobilacea (Juglandaceae). Int J Plant Sci 166:449–457

    Article  CAS  Google Scholar 

  • Li W-Y, Wu H-F (1978) A palynological investigation on the late Tertiary and early Quaternary and its significance in the paleogeographical study in central Yunnan. Acta Geograph Sin 33:142–155. doi:10.11821/xb197802005

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lu A-M (1982) On the geographical distribution of the Juglandaceae. Acta Phytotaxonomica Sin 20:257–274 (in Chinese)

    Google Scholar 

  • Lu A-M, Stone D, Grauke L (1999) Juglandaceae. In: Flora of China. Science Press, Beijing, pp 277–285

  • Luo R-S (2015) Systematics studies on endemic plants of Platycarya (Juglandacea) in eastern Asia. Guangxi Normal University, Guangxi

    Google Scholar 

  • Maechler M (2015) Diptest: Hartigan’s dip test statistic for unimodality corrected. R package version 0.75-7. Available at: https://CRAN.R-project.org/package=diptest

  • Manchester SR (1999) Biogeographical relationships of North American tertiary floras. Ann Mo Bot Gard:472–522

  • Manos PS, Stone DE (2001) Evolution, phylogeny, and systematics of the Juglandaceae. Ann Mo Bot Gard 88:231–269

    Article  Google Scholar 

  • Manos PS, Soltis PS, Soltis DE, Manchester SR, Oh SH, Bell CD, Dilcher DL, Stone DE (2007) Phylogeny of extant and fossil Juglandaceae inferred from the integration of molecular and morphological data sets. Syst Biol 56:412–430

    Article  PubMed  Google Scholar 

  • McCormack JE, Maley JM, Hird SM, Derryberry EP, Graves GR, Brumfield RT (2012) Next-generation sequencing reveals phylogeographic structure and a species tree for recent bird divergences. Mol Phylogenet Evol 62:397–406

    Article  PubMed  Google Scholar 

  • Ni J, Harrison SP, Prentice IC, Kutzbach JE, Sitch S (2006) Impact of climate variability on present and Holocene vegetation: a model-based study. Ecol Model 191:469–486

    Article  Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933–938

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2003) Documentation for structure software: version 2.3. J Pediatr Surg 41:55–63

    Google Scholar 

  • Pukk L, Ahmad F, Hasan S, Kisand V, Gross R, Vasemagi A (2015) Less is more: extreme genome complexity reduction with ddRAD using Ion Torrent semiconductor technology. Mol Ecol Resour 15:1145–1152

    Article  CAS  PubMed  Google Scholar 

  • Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature 407:180–182

    Article  CAS  PubMed  Google Scholar 

  • Qian H, Ricklefs RE (2001) Diversity of temperate plants in East Asia (Qian and Ricklefs reply). Nature 413:130

  • Qiu YX, Fu CX, Comes HP (2011) Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of Quaternary climate and environmental change in the world's most diverse temperate flora. Mol Phylogenet Evol 59:225–244

    Article  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Shen Z, Zhang X (2000) A quantitative analysis on the floristic elements of the Chinese subtropical region and their spatial patterns. Acta Phytotaxonomica Sin 38:366–380 (in Chinese)

    Google Scholar 

  • Shi M-M, Michalski SG, Welk E, Chen X-Y, Durka W, Carine M (2014) Phylogeography of a widespread Asian subtropical tree: genetic east-west differentiation and climate envelope modelling suggest multiple glacial refugia. J Biogeogr 41:1710–1720

    Article  Google Scholar 

  • Sun Y, Moore MJ, Yue L, Feng T, Chu H, Chen S, Ji Y, Wang H, Li J, Carine M (2014) Chloroplast phylogeography of the East Asian Arcto-Tertiary relict Tetracentron sinense (Trochodendraceae). J Biogeogr 41:1721–1732

    Article  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203

    Article  CAS  PubMed  Google Scholar 

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  CAS  PubMed  Google Scholar 

  • Tian S, Lei SQ, Hu W, Deng LL, Li B, Meng QL, Soltis DE, Soltis PS, Fan DM, Zhang ZY (2015) Repeated range expansions and inter-/postglacial recolonization routes of Sargentodoxa cuneata (Oliv.) Rehd. et Wils. (Lardizabalaceae) in subtropical China revealed by chloroplast phylogeography. Mol Phylogenet Evol 85:238–246

    Article  PubMed  Google Scholar 

  • Wan Q-C (2016) Phylogeography and population genetics of the East Asia endemic genus Platycarya (Juglandaceae). Ph.D. Thesis. Guangzhou: Sun Yat-sen University (in Chinese with English abstract)

  • Wang W-M (1996) A palynological survey of Neogene strata in Xiaolongtan basin, Yunnan province of south China. Acta Bot Sin 38:743–748 (in Chinese)

    Google Scholar 

  • Wang W-M, Chen G-J, Chen Y-F, Kuang G-D Tertiary palynostratigraphy of the Ningming basin, Guangxi. J Stratigr 27:324–327 (in Chinese)

  • Wang W, Shu J, Deng T (2009) Neogene pollen floras in China with regional orientation and environment response. Acta Palaeontol Sin 48:175–184 (in Chinese)

    Google Scholar 

  • Wang CB, Wang T, Su YJ (2014) Phylogeography of Cephalotaxus oliveri (Cephalotaxaceae) in relation to habitat heterogeneity, physical barriers and the uplift of the Yungui Plateau. Mol Phylogenet Evol 80:205–216

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplifications and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols. Academic Press, San Diego, pp 315–322

  • Whittemore AT, Schaal BA (1991) Interspecific gene flow in sympatric oaks. Proc Natl Acad Sci U S A 88:2540–2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wing SL, Hickey LJ (1984) The Platycarya perplex and the evolution of the Juglandaceae. Am J Bot 71:388–411

    Article  Google Scholar 

  • Wu CA, Campbell DR (2005) Cytoplasmic and nuclear markers reveal contrasting patterns of spatial genetic structure in a natural Ipomopsis hybrid zone. Mol Ecol 14:781–792

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Deng M, Jiang X-L, Westwood M, Song Y-G, Turkington R (2014) Phylogeography of Quercus glauca (Fagaceae), a dominant tree of east Asian subtropical evergreen forests, based on three chloroplast DNA interspace sequences. Tree Genet Genomes 11:805

    Article  Google Scholar 

  • Yu G, Chen X, Ni J et al (2000) Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. J Biogeogr 27:635–664

    Article  Google Scholar 

  • Zeng YF, Liao WJ, Petit RJ, Zhang DY (2011) Geographic variation in the structure of oak hybrid zones provides insights into the dynamics of speciation. Mol Ecol 20:4995–5011

    Article  PubMed  Google Scholar 

  • Zhang Z-H, Hu G, Zhu J-D, Luo D-H, Ni J (2010) Spatial patterns and interspecific associations of dominant tree species in two old-growth karst forests, SW China. Ecol Res 25:1151–1160

    Article  Google Scholar 

  • Zhang ZY, Wu R, Wang Q, Zhang ZR, Lopez-Pujol J, Fan DM, Li DZ (2013) Comparative phylogeography of two sympatric beeches in subtropical China: species-specific geographic mosaic of lineages. Ecol Evol 3:4461–4472

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng Z (2000) Late Quaternary vegetation and climatic changes in the tropical and subtropical areas of China. Acta Micropalaeontol Sin 17:125–146 (in Chinese)

    Google Scholar 

  • Zheng Z, Wei J, Huang K, Xu Q, Lu H, Tarasov P, Luo C, Beaudouin C, Deng Y, Pan A, Zheng Y, Luo Y, Nakagawa T, Li C, Yang S, Peng H, Cheddadi R (2014) East Asian pollen database: modern pollen distribution and its quantitative relationship with vegetation and climate. J Biogeogr 41:1819–1832

    Article  Google Scholar 

  • Zhong GL (2011) Afforestation techniques of indigenous tree species—Platycarya. Garden and Landscaping 1:53–54 (in Chinese)

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant no. 41230101), by the 7th Framework Program of the EC under the Trees4Future project (Trees4Future, 284181) and by the China Scholarship Council. The experiments dealing with the identification and genotyping of SNPs were performed at the Genome Transcriptome Facility of Bordeaux (grants from the Conseil Regional d’Aquitaine no. 20030304002FA and 20040305003FA and from the European Union, FEDER no. 2003227 and from Investissements d’avenir, Convention attributive d’aide EquipEx Xyloforest ANR-10-EQPX-16-01 and LabEx COTE ANR-10-LABX-45). The authors would like to thank Zhong Z. Zhou, Qiang Fan, Christophe Boury, Patrick Leger, Adline Delcamp and Mei L. Man for their help with the experiments. We also thank Zhe M. Hu, Yuan Z. Wu, Alexis Ducousso and members of the palynology team in Sun Yat-sen University for collecting the leaf samples. Thanks are also given to Olivier Lepais for guidance with the exploration of ddRAD sequence data and to the reviewers as well as to the associate editor for their constructive comments on earlier versions of this manuscript.

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Correspondence to Qiuchi Wan.

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Wan, Q., Zheng, Z., Huang, K. et al. Genetic divergence within the monotypic tree genus Platycarya (Juglandaceae) and its implications for species’ past dynamics in subtropical China. Tree Genetics & Genomes 13, 73 (2017). https://doi.org/10.1007/s11295-017-1153-9

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