Low genetic differentiation yet high phenotypic variation in the invasive populations of Spartina alterniflora in Guangxi, China

English version

Autoři: Fei-Fei Li ^aff001; Lu Gong ^aff001; Jun-Sheng Li ^aff001; Xiao-Yan Liu ^aff001; Cai-Yun Zhao ^aff001
Působiště autorů: State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, P.R. China ^aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222646

Souhrn

Genetic variation and population structure may reflect important information for invasion success of exotic plant species and thus help improve management of invasive plants. Spartina alterniflora is an invasive plant that is a major threat to the economy and environment of the coastal regions in China. We analyzed the genetic structure and diversity of six populations of S. alterniflora differing in invasion histories in Guangxi, China. A total of 176 individuals from the six populations produced 348 AFLP fragments. The average heterozygosity was significantly lower than in the native population. And genetic bottlenecks were also detected in most populations. Standardized F_ST statistics (Φpt = 0.015) and AMOVA results indicated weak genetic differentiation. Genetic admixture and obviously isolation by distance indicated populations in Guangxi come from a pre-admixed population by a single introduction. High phenotypic variations of S. alterniflora in Guangxi influenced by soil salinity and temperature might be an important reason for the successful invasion.

Klíčová slova:

Biology and life sciences – Evolutionary biology – Genetic polymorphism – Genetics – Population genetics – Phylogeography – Phenotypes – Heredity – Heterozygosity – Population biology – Ecology – Ecological metrics – Species diversity – Biogeography – Ecology and environmental sciences – Species colonization – Invasive species – People and places – Geographical locations – Asia – China – Earth sciences – Geography

Zdroje

1. Frankham R. Resolving the genetic paradox in invasive species. Heredity. 2005;94(4):385. doi: 10.1038/sj.hdy.6800634 15602569.

2. Roman J, Darling JA. Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol. 2007;22(9):454–64. doi: 10.1016/j.tree.2007.07.002 17673331.

3. Li Y, Stift M, van Kleunen M. Admixture increases performance of an invasive plant beyond first—generation heterosis. J Ecol. 2018;106(4):1595–606.

4. Hurka H, Bleeker W, Neuffer B. Evolutionary processes associated with biological invasions in the Brassicaceae. Biol Invasions. 2003;5(4):281–92.

5. Le Roux JJ, Wieczorek AM, Meyer J-Y. Genetic diversity and structure of the invasive tree Miconia calvescens in Pacific islands. Divers Distrib. 2008;14(6):935–48. doi: 10.1111/j.1472-4642.2008.00504.x

6. Thompson J, McNeilly T, Gay A. Population variation in Spartina anglica CE Hubbard: I. Evidence from a common garden experiment. New Phytol. 1991;117(1):115–28.

7. Wang Q, An S, Ma Z, Zhao B, Chen J, Li B. Invasive Spartina alterniflora: biology, ecology and management. Acta Phytotaxonomica Sinica. 2006;44(5):559–88.

8. Baisakh N, Subudhi PK, Arumuganathan K, Parco AP, Harrison SA, Knott CA, et al. Development and interspecific transferability of genic microsatellite markers in Spartina spp. with different genome size. Aquat Bot. 2009;91(4):262–6. doi: 10.1016/j.aquabot.2009.07.007

9. Utomo HS, Wenefrida I, Materne MD, Harrison SA. Genetic diversity and population genetic structure of saltmarsh Spartina alterniflora from four coastal Louisiana basins. Aquat Bot. 2009;90(1):30–6. doi: 10.1016/j.aquabot.2008.05.003

10. Ort BS, Thornton WJ. Changes in the population genetics of an invasive Spartina after 10 years of management. Biol Invasions. 2016;18(8):2267–81. doi: 10.1007/s10530-016-1177-3

11. Huska D, Leitch IJ, de Carvalho JF, Leitch AR, Salmon A, Ainouche M, et al. Persistence, dispersal and genetic evolution of recently formed Spartina homoploid hybrids and allopolyploids in Southern England. Biol Invasions. 2016;18(8):2137–51. doi: 10.1007/s10530-015-0956-6

12. Ainouche ML, Baumel A, Salmon A, Yannic G. Hybridization, polyploidy and speciation in Spartina (Poaceae). New Phytol. 2003;161(1):165–72. doi: 10.1046/j.1469-8137.2003.00926.x

13. Bernik BM, Li H, Blum MJ. Genetic variation of Spartina alterniflora intentionally introduced to China. Biol Invasions. 2016;18(5):1485–98. doi: 10.1007/s10530-016-1096-3

14. An S, Gu B, Zhou C, Wang Z, Deng Z, Zhi Y, et al. Spartina invasion in China: implications for invasive species management and future research. Weed Res. 2007;47(3):183–91.

15. Callaway JC, Josselyn MN. The introduction and spread of smooth cordgrass (Spartina alterniflora) in South San Francisco Bay. Estuaries. 1992;15(2):218–26.

16. Xiao D, Zhang L, Zhu Z. A study on seed characteristics and seed bank of Spartina alterniflora at saltmarshes in the Yangtze Estuary, China. Estuar Coast Shelf S. 2009;83(1):105–10. doi: 10.1016/j.ecss.2009.03.024

17. Chung C-H. Thirty years of ecological engineering with Spartina plantations in China. Ecol Eng. 1993;2(3):261–89.

18. Gan X, Cai Y, Choi C, Ma Z, Chen J, Li B. Potential impacts of invasive Spartina alterniflora on spring bird communities at Chongming Dongtan, a Chinese wetland of international importance. Estuar Coast Shelf S. 2009;83(2):211–8. doi: 10.1016/j.ecss.2009.03.026

19. Li B, Liao C-h, Zhang X-d, Chen H-l, Wang Q, Chen Z-y, et al. Spartina alterniflora invasions in the Yangtze River estuary, China: An overview of current status and ecosystem effects. Ecol Eng. 2009;35(4):511–20. doi: 10.1016/j.ecoleng.2008.05.013

20. Blum MJ, Sloop CM, Ayres DR, Strong DR. Characterization of microsatellite loci in Spartina species (Poaceae). Mol Ecol Notes. 2003;4(1):39–42. doi: 10.1046/j.1471-8286.2003.00556.x

21. Strong DR, Ayres DA. Control and consequences of Spartina spp. invasions with focus upon San Francisco Bay. Biol Invasions. 2016;18(8):2237–46. doi: 10.1007/s10530-015-0980-6

22. Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, et al. Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot. 2008;95(6):713–9. doi: 10.3732/ajb.2007358 21632397.

23. Deng Z, An S, Zhou C, Wang Z, Zhi Y, Wang Y, et al. Genetic structure and habitat selection of the tall form Spartina alterniflora Loisel. in China. Hydrobiologia. 2007;583(1):195–204. doi: 10.1007/s10750-006-0529-x

24. Xia L, Zhao H, Yang W, An S. Genetic diversity, ecotype hybrid, and mixture of invasive Spartina alterniflora Loisel in Coastal China. CLEAN–Soil, Air, Water. 2015;43(12):1672–81.

25. Ellstrand NC, Schierenbeck KA. Hybridization as a stimulus for the evolution of invasiveness in plants. Euphytica. 2006;148:35–46. doi: 10.1073/pnas.97.13.704310.1007/s10681-006-5939-3

26. Schierenbeck KA, Ellstrand NC. Hybridization and the evolution of invasiveness in plants and other organisms. Biol Invasions. 2008;11(5):1093–105. doi: 10.1007/s10530-008-9388-x

27. Rius M, Darling JA. How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol. 2014;29(4):233–42. doi: 10.1016/j.tree.2014.02.003 24636862.

28. Castillo JM, Gallego‐Tévar B, Figueroa E, Grewell BJ, Vallet D, Rousseau H, et al. Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America. Ecol Evol. 2018;8(10):4992–5007. doi: 10.1002/ece3.4063 29876076

29. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 2006;9(8):981–93. doi: 10.1111/j.1461-0248.2006.00950.x 16913942

30. Wang SP, Althoff DM. Phenotypic plasticity facilitates initial colonization of a novel environment. Evolution. 2019;73(2):303–16. doi: 10.1111/evo.13676 30618131

31. Zhao X, Zhao C, Liu X, Gong L, Deng Z, Li J. Growth characteristics and adaptability of Spartina alterniflora in different latitude area along China coast. Ecol. Sci. 2015;34:119–28.

32. Liu W, Strong DR, Pennings SC, Zhang Y. Provenance‐by‐environment interaction of reproductive traits in the invasion of Spartina alterniflora in China. Ecology. 2017;98(6):1591–9. doi: 10.1002/ecy.1815 28316076

33. Mo Z, Fan H, Liu L. Investigation on smooth Cordgrass (Spartina alterniflora) along Guangxi coastal tidal zone. Guangxi Sci. 2010;17(2):170–4.

34. Caiyun Z, Junsheng L, Xiangjian Z. Invasion and management of Spartina alterniflora along China's Coast. Beijing: Science Press; 2015.

35. Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 1995;23(21):4407–14. doi: 10.1093/nar/23.21.4407 7501463

36. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012;28:2537–9. doi: 10.1093/bioinformatics/bts460 22820204

37. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35(6):1547–9. doi: 10.1093/molbev/msy096 29722887

38. Pritchard J, Wen X, Falush D. Documentation for STRUCTURE software, version 2.3. University of Chicago, Chicago, IL. 2010.

39. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–20. doi: 10.1111/j.1365-294X.2005.02553.x 15969739

40. Earl DA. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012;4(2):359–61.

41. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007;23(14):1801–6. doi: 10.1093/bioinformatics/btm233 17485429

42. Rosenberg NA. DISTRUCT: a program for the graphical display of population structure. Mol Biol Evol. 2004;4(1):137–8.

43. Naegele RP, Tomlinson AJ, Hausbeck MK. Evaluation of a diverse, worldwide collection of wild, cultivated, and landrace pepper (Capsicum annuum) for resistance to phytophthora fruit rot, genetic diversity, and population structure. Phytopathology. 2015;105(1):110–8. doi: 10.1094/PHYTO-02-14-0031-R 25054617.

44. Karn E, Jasieniuk M. Genetic diversity and structure of Lolium perenne ssp. multiflorum in California vineyards and orchards indicate potential for spread of herbicide resistance via gene flow. Evol Appl. 2017;10(6):616–29. doi: 10.1111/eva.12478 28616068; PubMed Central PMCID: PMC5469165.

45. Cornuet JM, Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996;144(4):2001–14. 8978083

46. Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Biol Evol. 2006;6(1):288–95.

47. Oksanen J, Blanchet FG, Kindt R, Legendre P, O’hara R, Simpson GL, et al. Vegan: community ecology package. R package version 1.17–4. http://cran.r-project.org> Acesso em. 2010;23:2010.

48. Novy A, Smouse PE, Hartman JM, Struwe L, Honig J, Miller C, et al. Genetic Variation of Spartina alterniflora in the New York Metropolitan Area and Its Relevance for Marsh Restoration. Wetlands. 2010;30(3):603–8. doi: 10.1007/s13157-010-0046-6

49. Liu W, Maung-Douglass K, Strong DR, Pennings SC, Zhang Y, Mack R. Geographical variation in vegetative growth and sexual reproduction of the invasive Spartina alterniflora in China. J Ecol. 2016;104(1):173–81. doi: 10.1111/1365-2745.12487

50. Castillo JM, Gallego-Tevar B, Figueroa E, Grewell BJ, Vallet D, Rousseau H, et al. Low genetic diversity contrasts with high phenotypic variability in heptaploid Spartina densiflora populations invading the Pacific coast of North America. Ecol Evol. 2018;8(10):4992–5007. doi: 10.1002/ece3.4063 29876076; PubMed Central PMCID: PMC5980529.

51. Li J, Du L, Guan W, Yu F-H, van Kleunen M. Latitudinal and longitudinal clines of phenotypic plasticity in the invasive herb Solidago canadensis in China. Oecologia. 2016;182(3):755–64. doi: 10.1007/s00442-016-3699-x 27522606

52. Castillo JM, Grewell BJ, Pickart AJ, Figueroa E, Sytsma M. Variation in tussock architecture of the invasive cordgrass Spartina densiflora along the Pacific Coast of North America. Biol Invasions. 2016;18(8):2159–74. doi: 10.1007/s10530-015-0991-3

53. Dlugosch KM, Parker IM. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol. 2008;17(1):431–49. doi: 10.1111/j.1365-294X.2007.03538.x 17908213.

54. Facon B, Pointier J-P, Jarne P, Sarda V, David P. High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr biol. 2008;18(5):363–7. doi: 10.1016/j.cub.2008.01.063 18334202

55. Vivian-Smith G, Stiles EW. Dispersal of salt marsh seeds on the feet and feathers of waterfowl. Wetlands. 1994;14(4):316–9.

56. Grevstad FS, Strong DR, Garcia-Rossi D, Switzer RW, Wecker MS. Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results. Biol Control. 2003;27(1):32–42. doi: 10.1016/s1049-9644(02)00181-0

57. Davis HG, Taylor CM, Lambrinos JG, Strong DR. Pollen limitation causes an Allee effect in a wind-pollinated invasive grass (Spartina alterniflora). P Natl Acad Sci USA. 2004;101(38):13804–7. doi: 10.1073/pnas.0405230101 15317944; PubMed Central PMCID: PMC518837.

58. van Boheemen LA, Lombaert E, Nurkowski KA, Gauffre B, Rieseberg LH, Hodgins KA. Multiple introductions, admixture and bridgehead invasion characterize the introduction history of Ambrosia artemisiifolia in Europe and Australia. Mol Ecol. 2017;26(20):5421–34. doi: 10.1111/mec.14293 28802079

59. Cristescu ME. Genetic reconstructions of invasion history. Mol Ecol. 2015;24(9):2212–25. doi: 10.1111/mec.13117 25703061.

60. Kirwan ML, Guntenspergen GR, Morris JT. Latitudinal trends in Spartina alterniflora productivity and the response of coastal marshes to global change. Global Change Biol. 2009;15(8):1982–9.

61. Idaszkin YL, Bortolus A. Does low temperature prevent Spartina alterniflora from expanding toward the austral-most salt marshes? Plant Ecol. 2011;212(4):553–61.

62. Nestler J. Interstitial salinity as a cause of ecophenic variation in Spartina alterniflora. Estuar Coast Shelf S. 1977;5(6):707–14.

63. Guanmin H. The growth characteristics of Spartina alterniflora and relative competitive ability with Kandelia obovata in mangrove areas of Zhangjiang Estuary. Xiamen: Xiamen University; 2009.

Low genetic differentiation yet high phenotypic variation in the invasive populations of Spartina alterniflora in Guangxi, China

Souhrn

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