Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 45:16–23

    Article  Google Scholar 

  • Agrawal AF (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol Ecol Res 7:651–667

    Google Scholar 

  • Ando Y, Utsumi S, Ohgushi T (2010) Community structure of insect herbivores on introduced and native Solidago plants in Japan. Entomol Exp Appl 136:174–183

    Article  Google Scholar 

  • 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 31:632–641

    Article  Google Scholar 

  • Anstett NA, Naujokaitis-Lewis I, Johnson M (2014) Latitudinal gradients in herbivory on Oenothera biennis vary according to herbivore guild and specialization. Ecology 95:2915–2923

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Berenbaum MR, Zangerl AR (2006) Parsnip webworms and host plants at home and abroad: trophic complexity in a geographic mosaic. Ecology 87:3070–3081

    Article  Google Scholar 

  • 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 87:57–75

    Article  Google Scholar 

  • Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889

    Article  Google Scholar 

  • Cappuccino N, Root RB (1992) The significance of host patch edges to the colonization and development of Corythucha marmorata (Hemiptera, Tingidea). Ecol Entomol 17:109–113

    Article  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • Colautti RI, Maron JL, Barrett SCH (2009) Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evol Appl 2:187–199

    Article  Google Scholar 

  • Craig TP, Itami JK, Craig JV (2007) Host plant genotype influences survival of hybrids between Eurosta solidaginis host races. Evolution 61:2607–2613

    Article  Google Scholar 

  • Crawley MJ (1987) Plant ecology defended. Trends Ecol Evol 2:304

    Article  CAS  Google Scholar 

  • Elton C (1958) The ecology of invasions by animals and plants. Muthuen, London

    Book  Google Scholar 

  • Fox J, Weisberg S (2011) An {R} companion to applied regression, Second edition. Thousand Oaks, Sage, CA, USA

  • 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 191:528–535

    Article  CAS  Google Scholar 

  • Johnson MTJ, Agrawal AA (2005) Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–885

    Article  Google Scholar 

  • Kueffer C, Pyšek P, Richardson DM (2013) Integrative invasion science: model systems, multi-site studies, focused meta-analysis and invasion syndromes. New Phytol 200:615–633

    Article  Google Scholar 

  • Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Am Nat 168:E15–37

    Article  Google Scholar 

  • Lenth RV (2015) Using the lsmeans. R package version 2.21. https://www.jstatsoft.org/article/view/v069i01

  • 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 72:8–14

    Article  CAS  Google Scholar 

  • Maron JL, Vilá M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • 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 9:726–740

    Article  Google Scholar 

  • Moloney KA, Holzapfel C, Tielbörger K, Jeltsch Schurr FM (2009) Rethinking the common garden in invasion research. Perspect Plant Ecol 11:311–320

    Article  Google Scholar 

  • Nuismer SL, Gandon S (2008) Moving beyond common-garden and transplant designs: insight into the causes of local adaptation in species interactions. Am Nat 171:658–668

    PubMed  Google Scholar 

  • Orians CM, Ward D (2010) Evolution of plant defenses in nonindigenous environments. Annu Rev Entomol 55:439–459

    Article  CAS  Google Scholar 

  • 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 98:985–994

    Article  Google Scholar 

  • Paul ND, Hatcher PE, Taylor JE (2000) Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends Plant Sci 5:220–225

    Article  CAS  Google Scholar 

  • Poelman EH, Kessler A (2016) Keystone herbivores and the evolution of plant defenses. Trends Plant Sci 21:477–485

    Article  CAS  Google Scholar 

  • R Development Core Team (2016) R 3.3.2. R Foundation for statistical computing. Vienna, Austria. www.r-project.org

  • Root RB (1996) Herbivore pressure on goldenrods (Solidago altissima): its variation and cumulative effects. Ecology 77:1074–1087

    Article  Google Scholar 

  • 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 95:2569–2578

    Article  Google Scholar 

  • 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 128:909–921

    Article  Google Scholar 

  • 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 19:315–318

    Article  Google Scholar 

  • 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 98:2873–2884

    Article  Google Scholar 

  • Shimizu T (2003) Naturalized plants of Japan. In Heibonsha, Tokyo, Japan. (in Japanese)

  • Siemann E, Rogers WE (2003) Increased competitive ability of an invasive tree may be limited by an invasive beetle. Ecol Appl 13:1503–1507

    Article  Google Scholar 

  • 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:plw087

    Google Scholar 

  • Strauss SY, Sahli HF, Conner JK (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytol 165:81–90

    Article  Google Scholar 

  • Tack AJM, Ovaskainen O, Pulkkinen P, Roslin T (2010) Spatial location dominates over host plant genotype in structuring an herbivore community. Ecology 91:2660–2672

    Article  Google Scholar 

  • Uesugi A, Poelman EH, Kessler A (2013) A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae). Oecologia 173:1387–1396

    Article  Google Scholar 

  • Utsumi S, Ando Y, Craig TP, Ohgushi T (2011) Plant genotypic diversity increases population size of a herbivorous insect. Proc R Soc B 278:3108–3115

    Article  Google Scholar 

  • 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 82:149–168

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Center for Ecological Research, Kyoto University, Otsu, 520-2113, Japan

    Yuzu Sakata, Mito Ikemoto & Takayuki Ohgushi

  2. Department of Biological Environment, Akita Prefectural University, Akita, 010-0195, Japan

    Yuzu Sakata

  3. Department of Biology, University of Minnesota Duluth, Duluth, MN, 55812, USA

    Timothy P. Craig & Joanne K. Itami

  4. Uryu Experimental Forest, Field Science Center for Northern Biosphere, Hokkaido University, Horokanai, Hokkaido, 074-0741, Japan

    Shunsuke Utsumi

  5. Department of Life and Environmental Sciences, University of Tsukuba, Tsukuba, 305-8572, Japan

    Mito Ikemoto

Authors
  1. Yuzu Sakata
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timothy P. Craig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joanne K. Itami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mito Ikemoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shunsuke Utsumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takayuki Ohgushi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuzu Sakata.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 293 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sakata, Y., Craig, T.P., Itami, J.K. et al. Evolutionary and environmental effects on the geographical adaptation of herbivory resistance in native and introduced Solidago altissima populations. Evol Ecol 32, 547–559 (2018). https://doi.org/10.1007/s10682-018-9954-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-018-9954-3

Keywords

Search

Navigation