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Oecologia

pp 1–14 | Cite as

Founder effects, post-introduction evolution and phenotypic plasticity contribute to invasion success of a genetically impoverished invader

  • Zhi-Yong Liao
  • J. F. Scheepens
  • Qiao-Ming Li
  • Wei-Bin Wang
  • Yu-Long FengEmail author
  • Yu-Long ZhengEmail author
Population ecology – original research

Abstract

Multiple mechanisms may act synergistically to promote success of invasive plants. Here, we tested the roles of three non-mutually exclusive mechanisms—founder effects, post-introduction evolution and phenotypic plasticity—in promoting invasion of Chromolaena odorata. We performed a common garden experiment to investigate phenotypic diversification and phenotypic plasticity of the genetically impoverished invader in response to two rainfall treatments (ambient and 50% rainfall). We used ancestor–descendant comparisons to determine post-introduction evolution and the QST-FST approach to estimate past selection on phenotypic traits. We found that eight traits differed significantly between plants from the invasive versus native ranges, for two of which founder effects can be inferred and for six of which post-introduction evolution can be inferred. The invader experienced strong diversifying selection in the invasive range and showed clinal variations in six traits along water and/or temperature gradients. These clinal variations are likely attributed to post-introduction evolution rather than multiple introductions of pre-adapted genotypes, as most of the clinal variations were absent or in opposite directions from those for native populations. Compared with populations, rainfall treatments explained only small proportions of total variations in all studied traits for plants from both ranges, highlighting the importance of heritable phenotypic differentiation. In addition, phenotypic plasticity was similar for plants from both ranges although neutral genetic diversity was much lower for plants from the invasive range. Our results showed that founder effects, post-introduction evolution and phenotypic plasticity may function synergistically in promoting invasion success of C. odorata.

Keywords

Ancestor–descendant comparisons Chromolaena odorata Clinal changes Invasion mechanisms Local adaptation QST-FST approach Water stress 

Notes

Acknowledgements

We are grateful to Xiangqing Yu and Xiaona Shao for providing molecular data; Isabel Mück and Phillip Gienapp for sharing R code; Madalin Parepa for suggestions on data analysis. This work was supported by the National Key R&D Program of China (2017YFC1200101, 2016YFC1201100), the National Natural Science Foundation of China (31500463, 31470575, 31670545, 31270582), and a scholarship from the China Scholarship Council (201504910498).

Author contribution statement

ZYL and YLF conceived the ideas and designed experiments; ZYL, YLZ, WBW and QML collected the data; ZYL, JFS, and YLF analysed the data; ZYL wrote the first draft, with further inputs from JFS, YLZ and YLF.

Supplementary material

442_2019_4566_MOESM1_ESM.doc (680 kb)
Supplementary material 1 (DOC 679 kb)

References

  1. Alexander JM, Edwards PJ, Poll M, Parks CG, Dietz H (2009) Establishment of parallel altitudinal clines in traits of native and introduced forbs. Ecology 90:612–622CrossRefGoogle Scholar
  2. Banta JA, Richards CL (2018) Quantitative epigenetics and evolution. Heredity 121:210–224.  https://doi.org/10.1038/s41437-018-0114-x CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bastlova D, Kvet J (2002) Differences in dry weight partitioning and flowering phenology between native and non-native plants of purple loosestrife (Lythrum salicaria L.). Flora 197:332–340.  https://doi.org/10.1078/0367-2530-00049 CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Bhattarai GP, Meyerson LA, Anderson J, Cummings D, Allen WJ, Cronin JT (2017) Biogeography of a plant invasion: genetic variation and plasticity in latitudinal clines for traits related to herbivory. Ecol Monogr 87:57–75.  https://doi.org/10.1002/ecm.1233 CrossRefGoogle Scholar
  6. 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.  https://doi.org/10.1007/s00442-005-0070-z CrossRefPubMedGoogle Scholar
  7. Brommer J (2011) Whither P ST? The approximation of Q ST by P ST in evolutionary and conservation biology. J Evol Biol 24:1160–1168CrossRefGoogle Scholar
  8. Chun YJ, Le Corre V, Bretagnolle F (2011) Adaptive divergence for a fitness-related trait among invasive Ambrosia artemisiifolia populations in France. Mol Ecol 20:1378–1388.  https://doi.org/10.1111/j.1365-294X.2011.05013.x CrossRefPubMedGoogle Scholar
  9. Colautti RI, Lau JA (2015) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017CrossRefGoogle Scholar
  10. DeLucia EH, Maherali H, Carey EV (2000) Climate-driven changes in biomass allocation in pines. Glob Chang Biol 6:587–593.  https://doi.org/10.1046/j.1365-2486.2000.00338.x CrossRefGoogle Scholar
  11. Dlugosch KM, Parker IM (2008) Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol Lett 11:701–709.  https://doi.org/10.1111/j.1461-0248.2008.01181.x CrossRefPubMedGoogle Scholar
  12. Droogers P, Allen RG (2002) Estimating reference evapotranspiration under inaccurate data conditions. Irrig Drain Syst 16:33–45CrossRefGoogle Scholar
  13. Fan JW, Wang K, Harris W, Zhong HP, Hu ZM, Han B, Zhang WY, Wang JB (2009) Allocation of vegetation biomass across a climate-related gradient in the grasslands of Inner Mongolia. J Arid Environ 73:521–528.  https://doi.org/10.1016/j.jaridenv.2008.12.004 CrossRefGoogle Scholar
  14. Felker-Quinn E, Schweitzer JA, Bailey JK (2013) Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA). Ecol Evol 3:739–751.  https://doi.org/10.1002/ece3.488 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Feng YL, Lei YB, Wang RF, Callaway RM, Valiente-Banuet A, Inderjit Li YP, Zheng YL (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci USA 106:1853–1856.  https://doi.org/10.1073/pnas.0808434106 CrossRefPubMedGoogle Scholar
  16. Fisher RA, Williams M, Da Costa AL, Malhi Y, Da Costa RF, Almeida S, Meir P (2007) The response of an Eastern Amazonian rain forest to drought stress: results and modelling analyses from a throughfall exclusion experiment. Glob Chang Biol 13:2361–2378.  https://doi.org/10.1111/j.1365-2486.2007.01417.x CrossRefGoogle Scholar
  17. Geng Y, van Klinken RD, Sosa A, Li B, Chen J, Xu C-Y (2016) The relative importance of genetic diversity and phenotypic plasticity in determining invasion success of a clonal weed in the USA and China. Front Plant Sci 7:213PubMedPubMedCentralGoogle Scholar
  18. Goudet J (2014) Hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-14. http://www.unil.ch/popgen/softwares/hierfstat.htm
  19. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  20. Hirano M, Sakaguchi S, Takahashi K (2017) Phenotypic differentiation of the Solidago virgaurea complex along an elevational gradient: insights from a common garden experiment and population genetics. Ecol Evol 7:6949–6962.  https://doi.org/10.1002/ece3.3252 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866CrossRefGoogle Scholar
  22. Keller SR, Sowell DR, Neiman M, Wolfe LM, Taylor DR (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytol 183:678–690CrossRefGoogle Scholar
  23. Kilkenny FF, Galloway LF (2016) Evolution of marginal populations of an invasive vine increases the likelihood of future spread. New Phytol 209:1773–1780.  https://doi.org/10.1111/nph.13702 CrossRefPubMedGoogle Scholar
  24. Kriticos DJ, Yonow T, McFadyen RE (2005) The potential distribution of Chromolaena odorata (Siam weed) in relation to climate. Weed Res 45:246–254CrossRefGoogle Scholar
  25. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26CrossRefGoogle Scholar
  26. Lê S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18CrossRefGoogle Scholar
  27. Leger EA, Rice KJ (2007) Assessing the speed and predictability of local adaptation in invasive California poppies (Eschscholzia californica). J Evol Biol 20:1090–1103.  https://doi.org/10.1111/j.1420-9101.2006.01292.x CrossRefPubMedGoogle Scholar
  28. Li Y-P, Feng Y-L (2009) Differences in seed morphometric and germination traits of crofton weed (Eupatorium adenophorum) from different elevations. Weed Sci 57:26–30.  https://doi.org/10.1614/ws-08-068.1 CrossRefGoogle Scholar
  29. Liao ZY, Zhang R, Barclay GF, Feng YL (2013) Differences in competitive ability between plants from nonnative and native populations of a tropical invader relates to adaptive responses in abiotic and biotic environments. PLoS One 8:e71767.  https://doi.org/10.1371/journal.pone.0071767 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Liao ZY, Zheng YL, Lei YB, Feng YL (2014) Evolutionary increases in defense during a biological invasion. Oecologia 174:1205–1214.  https://doi.org/10.1007/s00442-013-2852-z CrossRefPubMedGoogle Scholar
  31. Liao ZY, Scheepens JF, Li WT, Wang RF, Zheng YL, Feng YL (2019) Biomass reallocation and increased plasticity might contribute to successful invasion of Chromolaena odorata. Flora 256:79–84.  https://doi.org/10.1016/j.flora.2019.05.004 CrossRefGoogle Scholar
  32. Lucek K, Sivasundar A, Seehausen O (2014) Disentangling the role of phenotypic plasticity and genetic divergence in contemporary ecotype formation during a biological invasion. Evolution 68:2619–2632CrossRefGoogle Scholar
  33. Malhi Y, Aragao L, Galbraith D, Huntingford C, Fisher R, Zelazowski P, Sitch S, McSweeney C, Meir P (2009) Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proc Natl Acad Sci USA 106:20610–20615.  https://doi.org/10.1073/pnas.0804619106 CrossRefPubMedGoogle Scholar
  34. Maron JL, Vila M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  35. Meimberg H, Hammond JI, Jorgensen CM, Park TW, Gerlach JD, Rice KJ, McKay JK (2006) Molecular evidence for an extreme genetic bottleneck during introduction of an invading grass to California. Biol Invasions 8:1355–1366.  https://doi.org/10.1007/s10530-005-2463-7 CrossRefGoogle Scholar
  36. Moloney KA, Holzapfel C, Tielbörger K, Jeltsch F, Schurr FM (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol Evol Syst 11:311–320CrossRefGoogle Scholar
  37. Nguyen MA, Ortega AE, Nguyen KQ, Kimball S, Goulden ML, Funk JL (2016) Evolutionary responses of invasive grass species to variation in precipitation and soil nitrogen. J Ecol 104:979–986.  https://doi.org/10.1111/1365-2745.12582 CrossRefGoogle Scholar
  38. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2.5-5. https://CRAN.R-project.org/package=vegan
  39. Qin R-M, Zheng Y-L, Valiente-Banuet A, Callaway RM, Barclay GF, Pereyra CS, Feng Y-L (2013) The evolution of increased competitive ability, innate competitive advantages, and novel biochemical weapons act in concert for a tropical invader. New Phytol 197:979–988CrossRefGoogle Scholar
  40. Schielzeth H, Nakagawa S (2013) Nested by design: model fitting and interpretation in a mixed model era. Methods Ecol Evol 4:14–24CrossRefGoogle Scholar
  41. Shao XN, Li QM, Lin LX, He TH (2018) On the origin and genetic variability of the two invasive biotypes of Chromolaena odorata. Biol Invasions.  https://doi.org/10.1007/s10530-018-1677-4 CrossRefGoogle Scholar
  42. Sultan SE (2000) Phenotypic plasticity for plant development, function and life history. Trends Plant Sci 5:537–542.  https://doi.org/10.1016/s1360-1385(00)01797-0 CrossRefPubMedGoogle Scholar
  43. te Beest M, Elschot K, Olff H, Etienne RS (2013) Invasion success in a marginal habitat: an experimental test of competitive ability and drought tolerance in Chromolaena odorata. PLoS One 8:e68274.  https://doi.org/10.1371/journal.pone.0068274 CrossRefGoogle Scholar
  44. Williams JL, Auge H, Maron JL (2008) Different gardens, different results: native and introduced populations exhibit contrasting phenotypes across common gardens. Oecologia 157:239–248CrossRefGoogle Scholar
  45. Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecol Monogr 82:149–168CrossRefGoogle Scholar
  46. Yu XQ, He TH, Zhao JL, Li QM (2014) Invasion genetics of Chromolaena odorata (Asteraceae): extremely low diversity across Asia. Biol Invasions 16:2351–2366.  https://doi.org/10.1007/s10530-014-0669-2 CrossRefGoogle Scholar
  47. Zachariades C, Day M, Muniappan R, Reddy G (2009) Chromolaena odorata (L.) King and Robinson (Asteraceae). Biological control of tropical weeds using arthropods. Cambridge University Press, Cambridge, pp 130–160CrossRefGoogle Scholar
  48. Zenni RD, Bailey JK, Simberloff D (2014) Rapid evolution and range expansion of an invasive plant are driven by provenance-environment interactions. Ecol Lett 17:727–735.  https://doi.org/10.1111/ele.12278 CrossRefPubMedGoogle Scholar
  49. Zheng YL, Liao ZY (2017) High-density native-range species affects the invasive plant Chromolaena odorata more strongly than species from its invasive range. Sci Rep 7:16075.  https://doi.org/10.1038/s41598-017-16376-4 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zheng YL, Feng YL, Zhang LK, Callaway RM, Valiente-Banuet A, Luo DQ, Liao ZY, Lei YB, Barclay GF, Silva-Pereyra C (2015) Integrating novel chemical weapons and evolutionarily increased competitive ability in success of a tropical invader. New Phytol 205:1350–1359.  https://doi.org/10.1111/nph.13135 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesMenglaChina
  2. 2.Plant Evolutionary Ecology, Institute of Evolution and EcologyUniversity of TübingenTübingenGermany
  3. 3.Liaoning Key Laboratory for Biological Invasions and Global Changes, College of Bioscience and BiotechnologyShenyang Agricultural UniversityShenyangChina
  4. 4.Center of Conservation Biology, Core Botanical GardensChinese Academy of SciencesMenglaChina

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