Evolution of invasiveness by genetic accommodation

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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.

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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.

Author information

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.

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) doi:10.1038/s41559-018-0553-z

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