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Multiple introductions and genetic admixture facilitate the successful invasion of Plantago virginica into China

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Abstract

Population genetic surveys can reveal the patterns of genetic diversity and provide insights into the details of invasion history. Plantago virginica L. (Plantaginaceae) is a North America species that was first reported in China in 1951 and has rapidly spread into the south-eastern areas of China. Although previous work has examined phenotypic variation during this invasion, the genetic variation and structure of P. virginica remains unclear. We used two chloroplast and seven microsatellite loci to analyse genetic diversity and population differentiation in 17 populations of P. virginica from the invaded range (China, n = 688) and 10 populations from its native range (USA, n = 625). Chloroplast haplotypes from all populations were clustered into two lineages (I and II) and invasive populations had 28 haplotypes, whereas native populations had only 10 haplotypes. DIYABC simulations based on microsatellite data also suggest multiple invasions into China. Invasive populations displayed high genetic diversity that was similar to that of the native range. However, there was markedly less genetic differentiation in Chinese populations (FST = 0.051) than in NA populations (FST = 0.143), suggesting increased gene flow within China. STRUCTURE analysis also revealed significant gene flow and lineage admixture among Chinese populations and MIGRATE analysis suggested high levels of gene flow to inland China from both the coast of China and populations in the United States. These results suggest that multiple introductions and genetic admixture likely play important roles in facilitating the invasion and geographic expansion of P. virginica into China.

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Data availability

Data from the current study are available from the corresponding author upon reasonable request, and the NCBI GenBank accession numbers are MW722451–MW722520.

References

  • Ahlstrand NI, Verstraete B, Hassemer G, Dunbar-Co S, Hoggard R, Meudt HM, Rønsted N (2019) Ancestral range reconstruction of remote oceanic island species of Plantago (Plantaginaceae) reveals differing scales and modes of dispersal. J Biogeogr 46:706–722

    Article  Google Scholar 

  • Allendorf FW, Lundquist LL (2003) Introduction: population biology, evolution, and control of invasive species. Conserv Biol 17:24–30

    Article  Google Scholar 

  • Amos W, Hoffman JI, Frodsham A, Zhang L, Best S, Hill AVS (2010) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Resour 7:10–14

    Article  CAS  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Barrett SCH, Husband BC (1990) Plant population genetics, breeding, and genetic resources. Sinauer, Sunderland, pp. 254–278

  • Beerli P, Palczewski M (2010) Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185:313–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Brown AHD, Marshall DR (1981) Evolutionary changes accompanying colonization in plants. Hunt Institute, Pittsburgh, pp. 351–363

  • Cornuet JM, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin JM, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism. DNA Seq Microsatell Data Bioinfo 30:187–1189

    Google Scholar 

  • Ding J, Mack RN, Lu L, Ren M, Huang H (2008) China’s booming economy is sparking and accelerating biological invasions. Bioscience 58:317–324

    Article  Google Scholar 

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? P Natl Acad Sci USA 97:7043–7050

    Article  CAS  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 

  • Excoffier L, Laval G, Schneider S (2007) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  PubMed Central  Google Scholar 

  • Fang F, Guo S, Huang H, Cao A (2004) Influences of population density of Plantago virginica on its morphological characters of underground and aboveground organs. J Trop Subtrop Bot 12:419–424

    Google Scholar 

  • Felker-Quinn E, Bailey JK, Schweitzer JA (2011) Soil biota drive expression of genetic variation and development of population-specific feedbacks in an invasive plant. Ecology 92:1208–1214

    Article  PubMed  Google Scholar 

  • Guo S, Gu D, Liu P, Hu Y (1996) Biological and ecological characteristics of Plantago virginica L. Acta Ecol Sin 16:302–307

    Google Scholar 

  • Guo SL, Fang F, Qiang S (2004) Studies on the reproduction and photosynthetic ecophysiology of the exotic invasive plant, Plantago virginica. Acta Phytoecol Sin 28:787–793

    Google Scholar 

  • Havrdová A, Douda J, Krak K, Vít P, Hadincová V, Zákravský P, Mandák B (2015) Higher genetic diversity in recolonized areas than in refugia of Alnus glutinosa triggered by continent-wide lineage admixture. Mol Ecol 24:4759–4777

    Article  PubMed  Google Scholar 

  • Hulme PE, Bacher S, Kenis M, Klotz S, Kühn I, Minchin D (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2010) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna RM, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  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 

  • Luo X, Xu X, Zheng Y, Guo H, Hu S (2019) The role of phenotypic plasticity and rapid adaptation in determining invasion success of Plantago virginica. Biol Invasions 21:2679–2692

    Article  Google Scholar 

  • Maebara Y, Tamaoki M, Iguchi Y, Nakahama N, Hayasaka D (2020) Genetic diversity of invasive Spartina alterniflora Loisel. (Poaceae) introduced unintentionally into japan and its invasion pathway. Front Plant Sci 11:1–12

    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 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao HM, Liu WW, Zhang YH, Zhang YY, Li QQ (2019) Genetic admixture accelerates invasion via provisioning rapid adaptive evolution. Mol Ecol 28:4012–4027

    Article  PubMed  Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J (2005) The tortoise and the hare: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    Article  CAS  PubMed  Google Scholar 

  • Sudhir K, Glen S, Koichiro T (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1884

    Article  CAS  Google Scholar 

  • Sun Y, Bossdorf O, Grados RD, Liao ZY, Müller-Schrer H (2020) Rapid genomic and phenotypic change in response to climate warming in a widespread plant invader. Glob Change Biol 26:6511–6522

    Article  Google Scholar 

  • Tang JS, Ma M (2020) Genetic diversity and genetic differentiation of invasive weed Xanthium italicum in China. CR Biol 343:63–72

    Google Scholar 

  • Vicente S, Cristina M, Trindade H (2018) Genetic diversity and differentiation of invasive Acacia longifolia in Portugal. Web Ecol 18:91–103

    Article  Google Scholar 

  • Wang HT, Zhou YM, Chen Y (2015) Allelopathic potential of invasive Plantago virginica on four lawn species. PLoS ONE 10:1–12

    Google Scholar 

  • Wang J, Gaughan S, Lamer JD, Deng C, Hu WT (2020) Resolving the genetic paradox of invasions: Preadapted genomes and post introduction hybridization of bigheaded carps in the Mississippi River Basin. Evol Appl 13:263–277

    Article  CAS  PubMed  Google Scholar 

  • Wang R, Wan FH (2010) Prediction of the potential survival area of Xanthium italicum in China. Acta Pratac Sin 6:222–230

    Google Scholar 

  • Wang XY, Shen DW, Jiao J, Xu NN, Yu S, Zhou XF (2012) Genotypic diversity enhances invasive ability of Spartina alterniflora. Mol Ecol 21:2542–2551

    Article  CAS  PubMed  Google Scholar 

  • White DM, Huang JP, Jara-Muoz OA, Madrián S, Mason-Gamer RJ (2021) The origins of coca: museum genomics reveals multiple independent domestications from progenitor Erythroxylum gracilipes. Syst Biol 70:1–13

    Article  CAS  PubMed  Google Scholar 

  • Xiao YA, Zhou B, Hu WH (2012) Differences in the selectivity of competitive strategy between Plantago virginica and P. asiatica in natural habitats. J JINGANGSHAN U (Nat Sci) 33:96–103

    Google Scholar 

  • Xu X, Luo X, Wang X, Guo H, Hu S (2017) Microsatellite primers in Plantago virginica (Plantaginaceae), an invasive species with both cleistogamous and chasmogamous flowers. Genes Genet Syst 92:293–297

    Article  PubMed  Google Scholar 

  • Xu X, Wolfe L, Diez J, Zheng Y, Guo H, Hu S (2019) Differential germination strategies of native and introduced populations of the invasive species Plantago virginica. NeoBiota 43:101–118

    Article  Google Scholar 

  • Young ND, Healy J (2003) GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinfo 4:6–12

    Article  Google Scholar 

  • Zhang DX, Liu LM, Guo SL (2010) Analysis of genetic diversity in Plantago virginica population. Weed Sci 2:14–17

    Google Scholar 

  • Zhang Y, Tang JS, Ren G, Zhao KX, Wang XF (2021) Global potential distribution prediction of Xanthium italicum based on Maxent model. Sci Rep 11:16545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31100298, U20A2080, 31622015) and Sichuan University (Fundamental Research Funds for the Central Universities, SCU2020D003, SCU2021D006). We thank Dr. Lei Shang, Meng Lu, Qiang Yang, Yazhu Liu and other colleagues for thier help and insightful discussions during the experimental processes. We are grateful to Prof. Zhiping Song for his very helpful suggestions.

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Author notes

  1. Jieshi Tang and Kangshan Mao contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, 610065, China

    Jieshi Tang, Kangshan Mao & Hongying Zhang

  2. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China

    Xinyu Xu & Hui Guo

  3. Laboratory Center of Life Sciences, College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Xiaohong Xu

  4. Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology and Centre for Invasion Biology, Institute of Biodiversity, School of Ecology and Environmental Science, Yunnan University, Kunming, 650504, Yunnan, China

    Bo Li

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  1. Jieshi Tang
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Contributions

JT and KM wrote the manuscript. XX and XX performed the experiments. JT and HZ performed the data analysis. HG and BL conceived and designed the experiments. KM and HG finalized the manuscript, all authors read and revised the manuscript.

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Correspondence to Hui Guo or Bo Li.

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Tang, J., Mao, K., Zhang, H. et al. Multiple introductions and genetic admixture facilitate the successful invasion of Plantago virginica into China. Biol Invasions 24, 2261–2272 (2022). https://doi.org/10.1007/s10530-022-02773-y

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  • DOI: https://doi.org/10.1007/s10530-022-02773-y

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