Evolution of invasiveness by genetic accommodation

Abstract

Invasion success of species introduced to novel environments may be facilitated by adaptive evolution and by phenotypic plasticity. Here we investigate the independent and joint contribution of both mechanisms as drivers of invasiveness in the perennial sunflower Helianthus tuberosus. We show that invasive genotypes have multiple origins, and that invasive spread was facilitated by the repeated evolution of extreme values in a single trait, clonality. In line with genetic accommodation theory, we establish that this evolutionary transition occurred by refining a preexisting plastic response of clonality to water availability. Further, we demonstrate that under the non-drought conditions typically experienced by this plant in its introduced range, invasive spread is mediated by hybrid vigour and/or two major additive-effect loci, and that these mechanisms are complementary. Thus, in H. tuberosus, evolution of invasiveness was facilitated by phenotypic plasticity, and involved the use of multiple genetic solutions to achieve the same invasiveness trait.

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Fig. 1: Population structure and genetic diversity of H.tuberosus.
Fig. 2: Phenotypic basis of invasiveness in H.tuberosus.
Fig. 3: Effect of environment on the contribution of clonality to invasiveness.
Fig. 4: Genetic architecture of tuber number production in H.tuberosus.
Fig. 5: Joint contribution of additive QTLs and heterozygosity to invasiveness.

References

  1. 1.

    Ellstrand, N. C. & Schierenbeck, K. A. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl Acad. Sci. USA 97, 7043–7050 (2000).

    Article  CAS  PubMed  Google Scholar 

  2. 2.

    Prentis, P. J., Wilson, J. R. U., Dormontt, E. E., Richardson, D. M. & Lowe, A. J. Adaptive evolution in invasive species. Trends Plant Sci. 13, 288–294 (2008).

    Article  CAS  PubMed  Google Scholar 

  3. 3.

    Bock, D. G. et al. What we still don’t know about invasion genetics. Mol. Ecol. 24, 2277–2297 (2015).

    Article  PubMed  Google Scholar 

  4. 4.

    Colautti, R. I. & Lau, J. A. Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol. Ecol. 24, 1999–2017 (2015).

    Article  PubMed  Google Scholar 

  5. 5.

    Tsutsui, N. D., Suarez, A. V., Holway, D. A. & Case, T. J. Reduced genetic variation and the success of an invasive species. Proc. Natl Acad. Sci. USA 97, 5948–5953 (2000).

    Article  CAS  PubMed  Google Scholar 

  6. 6.

    Perkins, T. A., Phillips, B. L., Baskett, M. L. & Hastings, A. Evolution of dispersal and life history interact to drive accelerating spread of an invasive species. Ecol. Lett. 16, 1079–1087 (2013).

    Article  PubMed  Google Scholar 

  7. 7.

    Dlugosch, K. M. & Parker, I. M. Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol. Lett. 11, 701–709 (2008).

    Article  PubMed  Google Scholar 

  8. 8.

    Colautti, R. I. & Barrett, S. C. Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342, 364–366 (2013).

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Krieger, M. J. B. & Ross, K. G. Identification of a major gene regulating complex social behavior. Science 295, 328–332 (2002).

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Gaines, T. A. et al. Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc. Natl Acad. Sci. USA 107, 1029–1034 (2010).

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Mueller, J. C. et al. Behaviour-related DRD4 polymorphisms in invasive bird populations. Mol. Ecol. 23, 2876–2885 (2014).

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Baker, H. The Genetics of Colonizing Species 147–168 (Academic Press, New York, 1965).

    Google Scholar 

  13. 13.

    Richards, C. L., Bossdorf, O., Muth, N. Z., Gurevitch, J. & Pigliucci, M. Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol. Lett. 9, 981–993 (2006).

    Article  PubMed  Google Scholar 

  14. 14.

    Davidson, A. M., Jennions, M. & Nicotra, A. B. Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol. Lett. 14, 419–431 (2011).

    Article  PubMed  Google Scholar 

  15. 15.

    West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, Oxford, 2003).

  16. 16.

    Crispo, E. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61, 2469–2479 (2007).

    Article  PubMed  Google Scholar 

  17. 17.

    Lande, R. Evolution of phenotypic plasticity in colonizing species. Mol. Ecol. 24, 2038–2045 (2015).

    Article  PubMed  Google Scholar 

  18. 18.

    Levis, N. A. & Pfennig, D. W. Evaluating ‘plasticity-first’ evolution in nature: key criteria and empirical approaches. Trends Ecol. Evol. 31, 563–574 (2016).

    Article  PubMed  Google Scholar 

  19. 19.

    Godoy, O., Valladares, F. & Pilar, C.-D. Multispecies comparison reveals that invasive and native plants differ in their traits but not in their plasticity. Funct. Ecol. 25, 1248–1259 (2011).

    Article  Google Scholar 

  20. 20.

    Bock, D. G., Kane, N. C., Ebert, D. P. & Rieseberg, L. H. Genome skimming reveals the origin of the Jerusalem artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phytol. 201, 1021–1030 (2014).

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    Baute, G. J., Owens, G. L., Bock, D. G. & Rieseberg, L. H. Genome-wide genotyping-by-sequencing data provide a high-resolution view of wild Helianthus diversity, genetic structure, and interspecies gene flow. Am. J. Bot. 103, 2170–2177 (2016).

    Article  PubMed  Google Scholar 

  22. 22.

    Kays, S. J. & Nottingham, S. F. Biology and Chemistry of the Jerusalem Artichoke: Helianthus tuberosus L. (CRC Press, Boca Raton, 2008).

    Google Scholar 

  23. 23.

    Konvalinková, P. in Plant Invasions: Ecological Threats and Management Solutions (ed. Child, L.) 289–299 (Backhuys, Leiden, 2003).

  24. 24.

    Fehér, A. Historical reconstruction of expansion of non-native plants in the Nitra River basin (SW Slovakia). Kanitzia 15, 47–62 (2007).

  25. 25.

    Balogh, L. in The Most Important Invasive Plants in Hungary ​(ed. Botta-Dukát, Z.) 227–255 (Hungarian Academy of Sciences Institute of Ecology and Botany, Vácrátót, 2008).

  26. 26.

    Filep, R., Balogh, L. & Csergö, A. M. Perennial Helianthus taxa in Târgu-Mureş city and its surroundings. J. Plant Dev. 17, 69–74 (2010).

    Google Scholar 

  27. 27.

    van Kleunen, M., Dawson, W., Schlaepfer, D. R., Jeschke, J. M. & Fischer, M. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecol. Lett. 13, 947–958 (2010).

    PubMed  Google Scholar 

  28. 28.

    Hollingsworth, M. L. & Bailey, J. P. Evidence for massive clonal growth in the invasive weed Fallopia japonica (Japanese knotweed). Bot. J. Linn. Soc. 133, 463–472 (2000).

  29. 29.

    Kliber, A. & Eckert, C. G. Interaction between founder effect and selection during biological invasion in an aquatic plant. Evolution 59, 1900–1913 (2005).

    CAS  PubMed  Google Scholar 

  30. 30.

    Zhang, Y.-Y., Zhang, D.-Y. & Barrett, S. C. H. Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol. Ecol. 19, 1774–1786 (2010).

    Article  CAS  PubMed  Google Scholar 

  31. 31.

    Dorken, M. E. & Eckert, C. G. Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J. Ecol. 89, 339–350 (2001).

    Article  Google Scholar 

  32. 32.

    Lippman, Z. B. & Zamir, D. Heterosis: revisiting the magic. Trends Genet. 23, 60–66 (2007).

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Keller, S. R. & Taylor, D. R. Genomic admixture increases fitness during a biological invasion. J. Evol. Biol. 23, 1720–1731 (2010).

    Article  CAS  PubMed  Google Scholar 

  34. 34.

    van Kleunen, M., Röckle, M. & Stift, M. Admixture between native and invasive populations may increase invasiveness of Mimulus guttatus. Proc. R. Soc. B 282, 20151487 (2015).

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    Hahn, M. A. & Rieseberg, L. H. Genetic admixture and heterosis may enhance the invasiveness of common ragweed. Evol. Appl. 10, 241–250 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Otto, S. P. The evolutionary consequences of polyploidy. Cell 131, 452–462 (2007).

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Flint-Garcia, S. A., Buckler, E. S., Tiffn, P., Ersoz, E. & Springer, N. M. Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS ONE 4, e7433 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Kantar, M. B. et al. Evaluating an interspecific Helianthus annuus × Helianthus tuberosus population for use in a perennial sunflower breeding program. Field Crops Res. 155, 254–264 (2014).

    Article  Google Scholar 

  39. 39.

    Ellstrand, N. C. et al. Crops gone wild: evolution of weeds and invasives from domesticated ancestors. Evol. Appl. 3, 494–504 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Hodgins, K. A. et al. Comparative genomics in the Asteraceae reveals little evidence for parallel evolutionary change in invasive taxa. Mol. Ecol. 24, 2226–2240 (2015).

    Article  CAS  PubMed  Google Scholar 

  41. 41.

    Qi, X. et al. More than one way to evolve a weed: parallel evolution of US weedy rice through independent genetic mechanisms. Mol. Ecol. 24, 3329–3344 (2015).

    Article  PubMed  Google Scholar 

  42. 42.

    Li, L.-F. et al. Signatures of adaptation in the weedy rice genome. Nat. Genet. 49, 811–814 (2017).

    Article  CAS  PubMed  Google Scholar 

  43. 43.

    Kolbe, J. J. et al. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431, 177–181 (2004).

    Article  CAS  PubMed  Google Scholar 

  44. 44.

    Jombart, T. & Ahmed, I. adegenet 1.3–1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Huson, D. H. Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267 (2005).

    Article  CAS  PubMed  Google Scholar 

  46. 46.

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

    Article  CAS  Google Scholar 

  47. 47.

    Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Earl, D. A. & von Holdt, B. M. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4, 359–361 (2012).

    Article  Google Scholar 

  49. 49.

    Francis, R. M. POPHELPER: an R package and web app to analyse and visualise population structure. Mol. Ecol. Resour. 17, 27–32 (2017).

    Article  CAS  PubMed  Google Scholar 

  50. 50.

    R Development Core Team R: A language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015).

  51. 51.

    Aulchenko, Y. S., Ripke, S., Isaacs, A. & van Duijn, C. M. GenABEL: an R library for genome-wide association analysis. Bioinformatics 23, 1294–1296 (2007).

    Article  CAS  PubMed  Google Scholar 

  52. 52.

    Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).

    Article  Google Scholar 

  53. 53.

    Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. nlme: Linear and Nonlinear Mixed Effects Models v. 3.1-131 (Comprehensive R Archive Network, 2017); http://CRAN.R-project.org/package=nlme

  54. 54.

    Hadfield, J. D. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  55. 55.

    Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).

    Google Scholar 

  56. 56.

    Hodgins, K. A. & Rieseberg, L. H. Genetic differentiation in life-history traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. J. Evol. Biol. 24, 2731–2749 (2011).

    Article  CAS  PubMed  Google Scholar 

  57. 57.

    Mayrose, M., Kane, N. C., Mayrose, I., Dlugosch, K. M. & Rieseberg, L. H. Increased growth in sunflower correlates with reduced defences and altered gene expression in response to biotic and abiotic stress. Mol. Ecol. 20, 4683–4694 (2011).

    Article  PubMed  Google Scholar 

  58. 58.

    Dlugosch, K. M. et al. Evolution of invasiveness through increased resource use in a vacant niche. Nat. Plants 1, 15066 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Kantar, M. B. et al. Ecogeography and utility to plant breeding of the crop wild relatives of sunflower (Helianthus annuus L.). Front. Plant Sci. 6, 841 (2015).

  60. 60.

    Walter, J., Essl, F., Englisch, T. & Kiehn, M. Neophytes in Austria: habitat preferences and ecological effects. Neobiota 6, 13–25 (2005).

    Google Scholar 

  61. 61.

    Descombes, P. et al. Monitoring and distribution modelling of invasive species along riverine habitats at very high resolution. Biol. Inv. 18, 3665–3679 (2016).

  62. 62.

    Petitpierre, B. et al. Climatic niche shifts are rare among terrestrial plant invaders. Science 335, 1344–1348 (2012).

  63. 63.

    Champely, S. pwr: Basic Functions for Power Analysis v. 1.2-0 (Comprehensive R Archive Network, 2012); http://CRAN.R-project.org/package=pwr

  64. 64.

    Rosyara, U. R., De Jong, W. S., Douches, D. S. & Endelman, J. B. Software for genome-wide association studies in autopolyploids and its application to potato. Plant Genome 9, 73 (2016).

  65. 65.

    Turner, S. D. qqman: an R package for visualizing GWAS results using QQ and Manhattan plots. Preprint at https://doi.org/10.1101/005165 (2014).

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Acknowledgements

Plant material used in this study was provided by L. Marek at the United States Department of Agriculture; D. Kessler and A. Diederichsen at Plant Gene Resources of Canada; M. Oppermann and H. Knuepffer at the Leibniz Institute of Plant Genetics and Crop Plant Research; and by N. Langlade and A. Zanetto at the French National Institute for Agricultural Research. We thank C. Bock, I. Bock, A. Bock, M. Bock, R. Filep and A. Stermin for help with sampling of invasive populations. We also thank C. Phillips, C. Tashlin Fluegel and C. Ramsay for assistance with DNA extractions and greenhouse work. The allelopathy bioassays were performed with the help of P. Qiao, A. Poon, S. Li, K. MacDonald, K. Borkowski and M. Iseminger. Also, we acknowledge M. Biron for assistance with greenhouse work, and A. Kuzmin for assistance with sequencing. The set-up and planting of the common garden was performed with help from M. Bock, S. Hubner, D. Burge, G. Baute, K. Stepien and S. Trehearne. The harvest of the common garden was performed with the help of M. Bock, O. Helmy, J. Brodie, S. Heredia, J. Henry, W. Cheung, K. Moran, M. Hahn, K. Ostevik, M. Todesco, E. Drummond, M. Pascual, J. Lee, K. Baute, A. Lalji, W. Choi, D. Skonieczny, I. Hamadi, V. Cha and C. Jewell. This work was supported by a Natural Sciences and Engineering Research Council (NSERC) Vanier CGS and a Killam Doctoral Fellowship to D.G.B., by the Swiss National Science Foundation (SNSF) Postdoctoral Fellowship P2FRP3_151662 to C.C., by the SNSF Doc.mobility Fellowship P1SKP3_168393 to R.M.-D. and by NSERC grant 327475 to L.H.R.

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Contributions

D.G.B. and L.H.R. conceived and planned the study. D.G.B. performed the sampling of invasive populations. D.G.B. and M.B.K. coordinated and conducted greenhouse plant propagations, common-garden fieldwork, and measurements of common-garden traits. D.G.B. and C.C. planned and conducted the bioassays that were used to quantify allelopathy. D.G.B. generated the GBS libraries and analysed the GBS data. R.M.-D. wrote the code and performed the analyses for trait differentiation among sample categories. D.G.B. performed the GWA mapping and the greenhouse drought experiment. All authors interpreted the results. D.G.B. wrote the paper with input from all authors.

Corresponding author

Correspondence to Dan G. Bock.

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Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Tables 2, 3, 6–8, 10–12, Supplementary Figures 1–10, Supplementary References

Reporting Summary

Supplementary Table 1

Sampling information for the H. tuberosus, H. grosseserratus, H. divaricatus and H. hirsutus accessions included in this study. The Site category column indicates, for the USDA-collected H. tuberosus accessions only,designation of sites as ‘artificial habitat’ or ‘natural habitat’ (see Classification of native, cultivated and invasive H. tuberosus section).

Supplementary Table 4

Results of mixed-ANOVAs with and without corrections for population structure for 13 common garden traits. Post hoc comparisons were performed for tests with significant Category term [native (N), invasive (I) and cultivated (C)] in the ‘lsmeans’ package. P values are corrected for multiple comparisons using the sequential Bonferroni method. Bold font indicates significance.

Supplementary Table 9

Clonal series identified for H. tuberosus samples. Details regarding sample IDs are given in Supplementary Table 1. For each clonal series, the highlight is used to indicate the sample included in the unique genotype set.

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Bock, D.G., Kantar, M.B., Caseys, C. et al. Evolution of invasiveness by genetic accommodation. Nat Ecol Evol 2, 991–999 (2018). https://doi.org/10.1038/s41559-018-0553-z

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