Evolutionary Ecology

, Volume 32, Issue 5, pp 547–559 | Cite as

Evolutionary and environmental effects on the geographical adaptation of herbivory resistance in native and introduced Solidago altissima populations

  • Yuzu SakataEmail author
  • Timothy P. Craig
  • Joanne K. Itami
  • Mito Ikemoto
  • Shunsuke Utsumi
  • Takayuki Ohgushi
Original Paper


To understand rapid evolution in plant resistance to herbivory, it is critical to determine how the genetic correlation among resistances varies genetically and/or environmentally. We conducted a reciprocal transplant experiment of tall goldenrod, Solidago altissima with multiple replicates within the native range (USA) and the introduced range (Japan) to explore the differences in phenotypic traits of resistance to multiple herbivorous insects and their relationships between and within the countries. The Japanese plants were more resistant to the lace bug, Corythucha marmorata, which had recently invaded Japan, but were more susceptible to other herbivorous insects compared to the USA plants. An antagonistic relationship was found between plant resistances to lace bugs and other herbivorous insects in both USA and Japanese plants. In addition, this relationship was more obvious in gardens with a high level of foliage damage than in gardens with a low level of foliage damage by other herbivorous insects. An antagonistic relationship between resistances to aphids and lace bugs was also observed in USA gardens, but not in Japanese garden. These results suggest that the strength of constraints on the evolution of plant resistance due to genetic trade-offs may differ among biotic environments, including community structure of herbivorous insects. Therefore, differences in herbivorous insect communities between the native and introduced ranges can result in the rapid evolution of greater resistance in plants in the introduced range than in the native range.


Biological invasion Plant-insect interaction Plant defense Reciprocal transplant experiment Solidago altissima 



We greatly appreciate T. Ida, K. Hashimoto, S. Hirano, S. Yamamura, M. Tokuda, S. Adachi, A. Yamasaki, and members of Laboratory of Systems Ecology in Saga University and Laboratory of Animal Ecology in Yamagata University for field work assistance. The present study was partly supported by the Japan Society for the Promotion of Science (JSPS) through Grant-Aid for Science Research (B-25291102) to T. O.

Supplementary material

10682_2018_9954_MOESM1_ESM.docx (292 kb)
Supplementary material 1 (DOCX 293 kb)


  1. Adachi S, Shirahama S, Tokuda M (2015) Seasonal occurrence of Uroleucon nigrotuberculatum (Hemiptera: Aphididae) in Northern Kyushu and mechanisms of its summer disappearance. Environ Entomol 45:16–23CrossRefGoogle Scholar
  2. Agrawal AF (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol Ecol Res 7:651–667Google Scholar
  3. Ando Y, Utsumi S, Ohgushi T (2010) Community structure of insect herbivores on introduced and native Solidago plants in Japan. Entomol Exp Appl 136:174–183CrossRefGoogle Scholar
  4. Ando Y, Utsumi S, Ohgushi T (2017) Aphid as a network creator for the plant-associated arthropod community and its consequence for plant reproductive success. Funct Ecol 31:632–641CrossRefGoogle Scholar
  5. Anstett NA, Naujokaitis-Lewis I, Johnson M (2014) Latitudinal gradients in herbivory on Oenothera biennis vary according to herbivore guild and specialization. Ecology 95:2915–2923CrossRefGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  7. Berenbaum MR, Zangerl AR (2006) Parsnip webworms and host plants at home and abroad: trophic complexity in a geographic mosaic. Ecology 87:3070–3081CrossRefGoogle Scholar
  8. Bhattarai GP, Meyerson LA, Anderson J, Cummings D, Allen WJ, Cronin JT (2016) Biogeography of a plant invasion: genetic variation and plasticity in latitudinal clines for traits related to herbivory. Ecol Monogr 87:57–75CrossRefGoogle Scholar
  9. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  10. Cappuccino N, Root RB (1992) The significance of host patch edges to the colonization and development of Corythucha marmorata (Hemiptera, Tingidea). Ecol Entomol 17:109–113CrossRefGoogle Scholar
  11. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  12. Colautti RI, Maron JL, Barrett SCH (2009) Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evol Appl 2:187–199CrossRefGoogle Scholar
  13. Craig TP, Itami JK, Craig JV (2007) Host plant genotype influences survival of hybrids between Eurosta solidaginis host races. Evolution 61:2607–2613CrossRefGoogle Scholar
  14. Crawley MJ (1987) Plant ecology defended. Trends Ecol Evol 2:304CrossRefGoogle Scholar
  15. Elton C (1958) The ecology of invasions by animals and plants. Muthuen, LondonCrossRefGoogle Scholar
  16. Fox J, Weisberg S (2011) An {R} companion to applied regression, Second edition. Thousand Oaks, Sage, CA, USAGoogle Scholar
  17. Halitschke R, Hamilton JG, Kessler A (2011) Herbivore-specific elicitation of photosynthesis by mirid bug salivary secretions in the wild tobacco Nicotiana attenuata. New Phytol 191:528–535CrossRefGoogle Scholar
  18. Johnson MTJ, Agrawal AA (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885CrossRefGoogle Scholar
  19. Kueffer C, Pyšek P, Richardson DM (2013) Integrative invasion science: model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytol 200:615–633CrossRefGoogle Scholar
  20. Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Am Nat 168:E15–37CrossRefGoogle Scholar
  21. Lenth RV (2015) Using the lsmeans. R package version 2.21.
  22. Maddox GD, Root RB (1987) Resistance to 16 diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia 72:8–14CrossRefGoogle Scholar
  23. Maron JL, Vilá M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280CrossRefGoogle Scholar
  24. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vázquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740CrossRefGoogle Scholar
  25. Moloney KA, Holzapfel C, Tielbörger K, Jeltsch Schurr FM (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol 11:311–320CrossRefGoogle Scholar
  26. Nuismer SL, Gandon S (2008) Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am Nat 171:658–668PubMedGoogle Scholar
  27. Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459CrossRefGoogle Scholar
  28. Parker JD, Torchin ME, Hufbauer RA, Lemoine NP, Alba C, Blumenthal DM, Bossdorf O, Byers JE, Dunn AM, Heckman RW, Hejda M, Jarosík V, Kanarek AR, Martin LB, Perkins SE, Pysek P, Schierenbeck K, Schlöder C, van Klinken R, Vaughn KJ, Williams W, Wolfe LM (2013) Do invasive species perform better in their new ranges? Ecology 98:985–994CrossRefGoogle Scholar
  29. Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225CrossRefGoogle Scholar
  30. Poelman EH, Kessler A (2016) Keystone herbivores and the evolution of plant defenses. Trends Plant Sci 21:477–485CrossRefGoogle Scholar
  31. R Development Core Team (2016) R 3.3.2. R Foundation for statistical computing. Vienna, Austria.
  32. Root RB (1996) Herbivore pressure on goldenrods (Solidago altissima): its variation and cumulative effects. Ecology 77:1074–1087CrossRefGoogle Scholar
  33. Sakata Y, Yamasaki M, Isagi Y, Ohgushi T (2014) An exotic herbivorous insect drives the evolution of resistance in the exotic perennial herb Solidago altissima. Ecology 95:2569–2578CrossRefGoogle Scholar
  34. Sakata Y, Itami J, Isagi Y, Ohgushi T (2015) Multiple and mass introductions from limited origins: genetic diversity and structure of Solidago altissima in the native and invaded range. J Plant Res 128:909–921CrossRefGoogle Scholar
  35. Sakata Y, Yamasaki M, Ohgushi T (2016) Urban landscape and forest vegetation regulate the range expansion of an exotic lace bug Corythucha marmorata (Hemiptera: Tingidae). Entomol Sci 19:315–318CrossRefGoogle Scholar
  36. Sakata Y, Craig TP, Itami JK, Yamasaki M, Ohgushi T (2017) Parallel environmental factors drive variation in insect density and plant resistance in the native and invaded ranges. Ecology 98:2873–2884CrossRefGoogle Scholar
  37. Shimizu T (2003) Naturalized plants of Japan. In Heibonsha, Tokyo, Japan. (in Japanese)Google Scholar
  38. Siemann E, Rogers WE (2003) Increased competitive ability of an invasive tree may be limited by an invasive beetle. Ecol Appl 13:1503–1507CrossRefGoogle Scholar
  39. Siemann E, DeWalt SJ, Zou J, Rogers WE (2017) An experimental test of the EICA Hypothesis in multiple ranges: invasive populations outperform those from the native range independent of insect herbivore suppression. AoB Plants 9:plw087Google Scholar
  40. Strauss SY, Sahli HF, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytol 165:81–90CrossRefGoogle Scholar
  41. Tack AJM, Ovaskainen O, Pulkkinen P, Roslin T (2010) Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology 91:2660–2672CrossRefGoogle Scholar
  42. Uesugi A, Poelman EH, Kessler A (2013) A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae). Oecologia 173:1387–1396CrossRefGoogle Scholar
  43. Utsumi S, Ando Y, Craig TP, Ohgushi T (2011) Plant genotypic diversity increases population size of a herbivorous insect. Proc R Soc B 278:3108–3115CrossRefGoogle Scholar
  44. Woods EC, Hastings A, 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

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Department of Biological EnvironmentAkita Prefectural UniversityAkitaJapan
  3. 3.Department of BiologyUniversity of Minnesota DuluthDuluthUSA
  4. 4.Uryu Experimental Forest, Field Science Center for Northern BiosphereHokkaido UniversityHorokanaiJapan
  5. 5.Department of Life and Environmental SciencesUniversity of TsukubaTsukubaJapan

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