Skip to main content
Log in

Standing variation boosted by multiple sources of introduction contributes to the success of the introduced species, Lotus corniculatus

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Although ecological differences between native and introduced ranges have been considered to drive rapid expansion of invasive species, recent studies suggest that rapid evolutionary responses of invasive species to local environments may also be common. Such expansion across heterogeneous environments by adaptation to local habitats requires genetic variation. In this study, we investigated the source and role of standing variation in successful invasion of heterogeneous abiotic environments in a self-incompatible species, Lotus corniculatus. We compared phenotypic and genetic variation among cultivars, natives, and introduced genotypes, and found substantial genetic variation within both native and introduced populations. Introduced populations possessed genotypes derived from both cultivars and native populations, and had lower population differentiation, indicating multiple sources of introduction and population admixture among the sources in the introduced range. Both cultivars and introduced populations had similarly outperforming phenotypes on average, with increased biomass and earlier flowering compared with native populations, but those phenotypes were within the range of the variation in phenotypes of the native populations. In addition, clinal variation within introduced populations was detected along a climatic gradient. Multiple introductions from different sources, including cultivars, may have contributed to pre-adaptive standing variation in the current introduced populations. We conclude that both introduction of cultivar genotypes and natural selection in local environments contributed to current patterns of genetic and phenotypic variation observed in the introduced populations.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23:38–44. doi:10.1016/j.tree.2007.09.008

    Article  PubMed  Google Scholar 

  • Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042. doi:10.1890/04-0341

    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 

  • Blumenthal DM, Hufbauer RA (2007) Increased plant size in exotic populations: a common-garden test with 14 invasive species. Ecology 88:2758–2765

    Article  PubMed  Google Scholar 

  • Bossdorf O, Prati D, Auge H et al (2004) Reduced competitive ability in an invasive plant. Ecol Lett 7:346–353

    Article  Google Scholar 

  • Bossdorf O, Auge H, Lafuma L et al (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11

    Article  PubMed  Google Scholar 

  • Cheptou PO, Carrue O, Rouifed S et al (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci USA 105:3796–3799

    Article  PubMed  CAS  Google Scholar 

  • Cody ML, Overton JM (1996) Short-term evolution of reduced dispersal in island plant populations. J Ecol 84:53–61

    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 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  PubMed  CAS  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Elam DR, Ridley CE, Goodell K et al (2007) Population size and relatedness affect fitness of a self-incompatible invasive plant. Proc Natl Acad Sci USA 104:549–552

    Article  PubMed  CAS  Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050

    Article  PubMed  CAS  Google Scholar 

  • Genton BJ, Shykoff JA, Giraud T (2005) High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction. Mol Ecol 14:4275–4285

    Article  PubMed  CAS  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Keller SR, Sowell DR, Neiman M et al (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytol 183:678–690

    Article  PubMed  Google Scholar 

  • Kitajima K, Fox AM, Sato T, Nagamatsu D (2006) Cultivar selection prior to introduction may increase invasiveness: evidence from Ardisia crenata. Biol Invasions 8:1471–1482

    Article  Google Scholar 

  • Kollmann J, Banuelos MJ (2004) Latitudinal trends in growth and phenology of the invasive alien plant Impatiens glandulifera (Balsaminaceae). Divers Distrib 10:377–385

    Article  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Li B, Suzuki J, Hara T (1998) Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana. Oecologia 115:293–301

    Google Scholar 

  • Li F, Bao W, Wu N et al (2008) Growth, biomass partitioning, and water-use efficiency of a leguminous shrub (Bauhinia faberi var. microphylla) in response to various water availabilities. New Forest 36:53–65

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • Maron JL, Vila M, Bommarco R et al (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280

    Article  Google Scholar 

  • Maron JL, Elmendorf SC, Vila M (2007) Contrasting plant physiological adaptation to climate in the native and introduced range of Hypericum perforatum. Evolution 61:1912–1924

    Article  PubMed  Google Scholar 

  • Mimura M, Aitken SN (2007) Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis. Heredity 99:224–232

    Article  PubMed  CAS  Google Scholar 

  • Mimura M, Aitken SN (2010) Local adaptation at the range peripheries of Sitka spruce. J Evol Biol 23:249–258

    Article  PubMed  CAS  Google Scholar 

  • Neuffer B, Hurka H (1999) Colonization history and introduction dynamics of Capsella bursa-pastoris (Brassicaceae) in North America: isozymes and quantitative traits. Mol Ecol 8:1667–1681

    Article  PubMed  Google Scholar 

  • Olsson K, Ågren J (2002) Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria. J Evol Biol 15:983–996

    Article  Google Scholar 

  • Pairon M, Petitpierre B, Campbell M et al (2010) Multiple introductions boosted genetic diversity in the invasive range of black cherry (Prunus serotina; Rosaceae). Ann Bot 105:881–890

    Article  PubMed  CAS  Google Scholar 

  • Parker IM (1997) Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub. Ecology 78:1457

    Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    PubMed  CAS  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE et al (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  PubMed  CAS  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993

    Article  PubMed  Google Scholar 

  • Ridley CE, Ellstrand NC (2009) Evolution of enhanced reproduction in the hybrid-derived invasive, California wild radish (Raphanus sativus). Biol Invasions 11:2251–2264

    Article  Google Scholar 

  • Roach DA, Wulff RD (2009) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

    Article  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B Biol Sci 273:2453–2459

    Article  Google Scholar 

  • Shaw J, Lickey EB, Schilling EE et al (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288

    Article  PubMed  CAS  Google Scholar 

  • Shimizu N, Morita H, Hirota S (2001) Japan invasive plant guide: plant invader 600 species. Zenkoku-Nouson-Kyouiku-Kyoukai, Tokyo

    Google Scholar 

  • Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4:514–518

    Article  Google Scholar 

  • 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 

  • Steiner JJ, de los Santos GG (2001) Adaptive ecology of Lotus corniculatus L. genotypes: I. Plant morphology and RAPD maker characterizations. Crop Sci 41:552–563

    Article  Google Scholar 

  • Taberlet P, Gielly L, Pautou G et al (1991) Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  • Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, “invasive traits” and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580

    Article  Google Scholar 

  • Whitney KD, Randell RA, Rieseberg LH (2010) Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 187:230–239

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank N. Kaneko and K. Hiratsuka for their useful suggestions and access to facilities during our experiments, and R. Kitagawa, A. Ohta, and K. Miura for technical assistance. We are also grateful to GRIN-USDA and Unzen-Amakusa National Parks of Japan for their kind understanding and cooperation for making seed collections possible. This research was supported by the GCOE program for ecological risk management at Yokohama National University and Grants-in-Aid for Scientific Research from Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Mimura.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1294 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mimura, M., Ono, K., Goka, K. et al. Standing variation boosted by multiple sources of introduction contributes to the success of the introduced species, Lotus corniculatus . Biol Invasions 15, 2743–2754 (2013). https://doi.org/10.1007/s10530-013-0488-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0488-x

Keywords

Navigation