Skip to main content
SpringerLink
Log in

Genetic and geographic structure of an insect resistant and a susceptible type of Barbarea vulgaris in western Europe

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

Abstract

Interactions between herbivores and plants are believed to have been important drivers of biodiversity. However, to drive an initial resistance divergence into different evolutionary lineages and taxa, these interactions have probably been embedded in other processes of divergence, like allopatric isolation. The cruciferous plant Barbarea vulgaris ssp. arcuata occurs in Denmark in two types: one (G) is resistant to most genotypes of the flea beetle Phyllotreta nemorum, the other (P) is susceptible. The two types additionally differ in hairiness and glucosinolates, they are genetically strongly divergent, and reproduction between them is reduced. To determine whether the two plant types and their resistance polymorphisms are also present outside Denmark, and to understand how they have evolved, we analysed 33 European populations of B. vulgaris for resistance, hairiness, glucosinolates, and microsatellite markers. Most populations had traits indicative of the G type, including the already characterized Danish G populations. In contrast, only two populations outside Denmark were of the P type; one from northern Sweden and one from Estonia. Genetically, the G populations formed two genetic clusters that were strongly divergent from a genetic cluster containing P populations. A fourth genetic cluster, which contained only a single population and no Danish plants, belonged morphologically to the subspecies ssp. vulgaris. The divergence found in Denmark between a resistant G and a susceptible P type is thus part of a larger divergence in Europe. Judging from the trait correlations, genetic divergence, and partial reproductive incompatibility, the plant types must have been isolated from each other for quite some time. The two P populations outside Denmark came from the north and east, suggesting a more eastern distribution. If so, resistant and susceptible types could have diverged during the ice age and later met in Scandinavia. However, more samples from Eastern Europe are needed to clarify this.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agerbirk N, Olsen CE, Nielsen JK (2001) Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58:91–100

    Article  PubMed  CAS  Google Scholar 

  • Agerbirk N, Ørgaard M, Nielsen JK (2003) Glucosinolates, flea beetle resistance, and leaf pubescence as taxonomic characters in the genus Barbarea (Brassicaceae). Phytochemistry 63:69–80

    Article  PubMed  CAS  Google Scholar 

  • Allen GC, Flores-Vergara MA, Krasnyanski S, Kumar S, Thompson WF (2006) A modified protocol for rapid DNA isolation from plant tissues using cetyltrimethylammonium bromide. Nat Protoc 1:2320–2325

    Article  PubMed  CAS  Google Scholar 

  • Allmon WD (1992) A causal analysis of stages in allopatric speciation. Oxford Surveys in Evolutionary Biology 8:219–257

    Google Scholar 

  • Besnard G, Basic N, Christin PA, Savova-Bianchi D, Galland N (2009) Thlaspi caerulescens (Brassicaceae) population genetics in western Switzerland: is the genetic structure affected by natural variation of soil heavy metal concentrations? New Phytol 181:974–984

    Article  PubMed  CAS  Google Scholar 

  • Bhagwat SA, Willis KJ (2008) Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits? J Biogeogr 35:464–482

    Article  Google Scholar 

  • Borgen L, Hultgard UM (2003) Parnassia palustris: a genetically diverse species in Scandinavia. Bot J Linn Soc 142:347–372

    Article  Google Scholar 

  • Breedlove D, Ehrlich PR (1968) Plant—herbivore coevolution—lupines and Lycaenids. Science 162:671–672

    Article  PubMed  CAS  Google Scholar 

  • Clauss MJ, Mitchell-Olds T (2006) Population genetic structure of Arabidopsis lyrata in Europe. Mol Ecol 15:2753–2766

    Article  PubMed  CAS  Google Scholar 

  • Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843

    Article  PubMed  Google Scholar 

  • Crawford NG (2010) Smogd: software for the measurement of genetic diversity. Molecular Ecology Resources 10:556–557

    Article  PubMed  Google Scholar 

  • Dalby-Brown L, Olsen CE, Nielsen JK, Agerbirk N (2011) Polymorphism for novel tetraglycosylated flavonols in an eco-model crucifer, Barbarea vulgaris. J Agric Food Chem. (in press). doi:10.1021/jf200412c

  • De Carvalho D, Ingvarsson PK, Joseph J, Suter L, Sedivy C, Macaya-Sanz D, Cottrell J, Heinze B, Schanzer I, Lexer C (2010) Admixture facilitates adaptation from standing variation in the European aspen (Populus tremula L.), a widespread forest tree. Mol Ecol 19:1638–1650

    Article  Google Scholar 

  • de Jong PW, Nielsen JK (1999) Polymorphism in a flea beetle for the ability to use an atypical host plant. Proc R Soc Lond B Biol Sci 266:103–111

    Article  Google Scholar 

  • de Jong PW, Frandsen HO, Rasmussen L, Nielsen JK (2000) Genetics of resistance against defences of the host plant Barbarea vulgaris in a Danish flea beetle population. Proc R Soc Lond B Biol Sci 267:1663–1670

    Article  Google Scholar 

  • de Jong PW, Breuker CJ, de Vos H, Vermeer KMCA, Oku K, Verbaarschot P, Nielsen JK, Brakefield PM (2009) Genetic differentiation between resistance phenotypes in the phytophagous flea beetle, Phyllotreta nemorum. J Insect Sci 9:article 69

    Google Scholar 

  • Dres M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philos Trans R Soc Lond B Biol Sci 357:471–492

    Article  PubMed  Google Scholar 

  • Edmunds GF, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945

    Article  PubMed  Google Scholar 

  • Feder JL, Filchak KE (1999) It’s about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Entomol Exp Appl 91:211–225

    Article  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  • Flannery ML, Mitchell FJG, Coyne S, Kavanagh TA, Burke JI, Salamin N, Dowding P, Hodkinson TR (2006) Plastid genome characterisation in Brassica and Brassicaceae using a new set of nine SSRs. Theor Appl Genet 113:1221–1231

    Article  PubMed  CAS  Google Scholar 

  • Fremstad E, Pedersen O (2009) Alien plants in Norway. Winter-cress Barbarea vulgaris (in Norwegian). Blyttia 67:159

    Google Scholar 

  • Futuyma DJ, Agrawal AA (2009) Macroevolution and the biological diversity of plants and herbivores. Proc Natl Acad Sci USA 106:18054–18061

    Article  PubMed  CAS  Google Scholar 

  • Geraci A, Chevre AM, Divaret I, Eber F, Raimondo FM (2004) Isozyme analysis of genetic diversity in wild Sicilian populations of Brassica sect. Brassica in view of genetic resources management. Genet Resour Crop Evol 51:137–146

    Article  CAS  Google Scholar 

  • Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on G(st) and D: forget G(st) but not all of statistics!. Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Glemin S, Gaude T, Guillemin ML, Lourmas M, Olivieri I, Mignot A (2005) Balancing selection in the wild: testing population genetics theory of self-incompatibility in the rare species Brassica insularis. Genetics 171:279–289

    Article  PubMed  CAS  Google Scholar 

  • Guillot G, Santos F, Estoup A (2008) Analysing georeferenced population genetics data with Geneland: a new algorithm to deal with null alleles and a friendly graphical user interface. Bioinformatics 24:1406–1407

    Article  PubMed  CAS  Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    PubMed  CAS  Google Scholar 

  • Heller R, Siegismund HR (2009) Relationship between three measures of genetic differentiation G(st), D(est) and G’(st): How wrong have we been? Mol Ecol 18:2080–2083

    Article  PubMed  CAS  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Jensen J (1985) Brassicaceae. In: Hansen K (ed) Dansk Feltflora. Gyldendal, Copenhagen, pp 225–252

    Google Scholar 

  • Jost L (2008) G(ST) and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kuzina V, Ekstrom CT, Andersen SB, Nielsen JK, Olsen CE, Bak S (2009) Identification of defense compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an ecometabolomic approach. Plant Physiol 151:1977–1990

    Article  PubMed  CAS  Google Scholar 

  • Kuzina V, Nielsen JK, Augustin JM, Torp AM, Bak S, Andersen SB (2011) Barbarea vulgaris linkage map and quantitative trait loci for saponins, glucosinolates, hairiness and resistance to the herbivore Phyllotreta nemorum. Phytochemistry 72:188–198

    Article  PubMed  CAS  Google Scholar 

  • Lyshede OB (2006) Korsblomstfamilien, Brassicaceae. In: Frederiksen S, Rasmussen FN, Seberg O (eds) Dansk Flora. Gyldendal, Copenhagen

    Google Scholar 

  • Macdonald MA, Cavers PB (1991) The biology of Canadian weeds 97. Barbarea vulgaris R Br. Can J Plant Sci 71:149–166

    Article  Google Scholar 

  • Meirmans PG, Hedrick PW (2011) Assessing population structure: F-st and related measures. Mol Ecol Resour 11:5–18

    Article  PubMed  Google Scholar 

  • Nielsen JK (1997) Variation in defences of the plant Barbarea vulgaris and in counteradaptations by the flea beetle Phyllotreta nemorum. Entomol Exp Appl 82:25–35

    Article  Google Scholar 

  • Nielsen JK (1999) Specificity of a Y-linked gene in the flea beetle Phyllotreta nemorum for defences in Barbarea vulgaris. Entomol Exp Appl 91:359–368

    Article  Google Scholar 

  • Nielsen JK, de Jong PW (2005) Temporal and host-related variation in frequencies of genes that enable Phyllotreta nemorum to utilize a novel host plant, Barbarea vulgaris. Entomol Exp Appl 115:265–270

    Article  Google Scholar 

  • Nordström S, Hedren M (2008) Genetic differentiation and postglacial migration of the Dactylorhiza majalis ssp. traunsteineri/lapponica complex into Fennoscandia. Plant Syst Evol 276:73–87

    Article  Google Scholar 

  • Nyman T, Vikberg V, Smith DR, Boeve JL (2010) How common is ecological speciation in plant-feeding insects? A ‘higher’ Nematinae perspective. BMC Evol Biol 10

  • Ørgaard M, Linde-Laursen IB (2007) Cytogenetics of Danish species of Barbarea (Brassicaceae): chromocentres, chromosomes and rDNA sites. Hereditas 144:159–170

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B, Deans JD, Espinel S, Fineschi S, Finkeldey R, Glaz I, Goicoechea PG, Jensen JS, König AO, Lowe AJ, Madsen SF, Mátyás G, Munro RC, Popescu F, Slade D, Tabbener H, de Vries SGM, Ziegenhagen B, de Beaulieu J-L, Kremer A (2002) Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manage 156:49–74

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) Genepop (version-1.2)—population-genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Renwick JAA (2002) The chemical world of crucivores: lures, treats and traps. Entomol Exp Appl 104:35–42

    Article  CAS  Google Scholar 

  • Rich T (1987) The genus Barbarea R.Br. (Cruciferae) in Britain and Ireland. Watsonia 16:389–396

    Google Scholar 

  • Rich TCG (1991) Crucifers of Great Britain and Ireland. BSBI Handbook No 6. Botanical Society of the British Isles, London

  • Rich KA, Thompson JN, Fernandez CC (2008) Diverse historical processes shape deep phylogeographical divergence in the pollinating seed parasite Greya politella. Mol Ecol 17:2430–2448

    Article  PubMed  CAS  Google Scholar 

  • Rundell RJ, Price TD (2009) Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends Ecol Evol 24:394–399

    Article  PubMed  Google Scholar 

  • Shinoda T, Nagao T, Nakayama M, Serizawa H, Koshioka M, Okabe H, Kawai A (2002) Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella. J Chem Ecol 28:587–599

    Article  PubMed  CAS  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Song BH, Clauss MJ, Pepper A, Mitchell-Olds T (2006) Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis. Mol Ecol 15:357–369

    Article  PubMed  CAS  Google Scholar 

  • Stewart JR, Lister AM, Barnes I, Dalen L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B Biol Sci 277:661–671

    Article  Google Scholar 

  • Summers K, Amos W (1997) Behavioral, ecological, and molecular genetic analyses of reproductive strategies in the Amazonian dart-poison frog, Dendrobates ventrimaculatus. Behav Ecol 8:260–267

    Article  Google Scholar 

  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    Article  PubMed  CAS  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Toneatto F (2009) Genetics and distribution of insect resistance polymorphism in Barbarea vulgaris. University of Copenhagen, Frederiksberg

    Google Scholar 

  • Toneatto F, Nielsen JK, Ørgaard M, Hauser TP (2010) Genetic and sexual separation between insect resistant and susceptible Barbarea vulgaris plants in Denmark. Mol Ecol 19:3456–3465

    Article  PubMed  CAS  Google Scholar 

  • Vähä JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72

    Article  PubMed  Google Scholar 

  • van Leur H, Raaijmakers CE, van Dam NM (2006) A heritable glucosinolate polymorphism within natural populations of Barbarea vulgaris. Phytochemistry 67:1214–1223

    Article  PubMed  Google Scholar 

  • Van Rossum F, Prentice HC (2004) Structure of allozyme variation in Nordic Silene nutans (Caryophyllaceae): population size, geographical position and immigration history. Biol J Linn Soc 81:357–371

    Article  Google Scholar 

  • Vercken E, Fontaine MC, Gladieux P, Hood ME, Jonot O, Giraud T (2010) Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica. PLoS Pathog 6:e1001229

    Article  PubMed  CAS  Google Scholar 

  • Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806–815

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Seeds were kindly provided from Akademia Medyczna Gdansk, Arboretum National de Chevrelup, Botanicki Vrt. Zagreb, Botanisher Garten Berlin Dahlem, Botanisher Garten Der Universität Graz, Botanisher Garten St. Gallen, Botanisher Garten Westf. Wilhelms Universität Münster, Giardino Botanico dell’Università di Urbino, Grădina Botanică Anastasie Fătulasi, Hanneke van Leur, Jardim Botânico da Universidade de Coimbra, Jardin Botanique Nantes, Ringve Botanical Garden, Universität Bayreuth Botanisher Garten, Universität Rostok Botanisher Garten, University of Oulu Botanical Garden. Heidi Rønde Olsen did the HPLC analyses of glucosinolates and helped with resistance bio-assays, and Mai-Britt Sauer helped maintaining the plants. This work was carried out as part of Fiorello Toneattos PhD project, funded by the Royal Veterinary and Agricultural University (now Faculty of Life Sciences, University of Copenhagen). Furthermore, the project was funded by grants from The Danish Agency for Science, Technology and Innovation (274-06-0370 and 274-08-0462).

Author information

Authors and Affiliations

  1. Department of Agriculture and Ecology, University of Copenhagen, Rolighedsvej 21, 4000, Frederiksberg, Denmark

    T. P. Hauser & F. Toneatto

  2. Department of Basic Sciences and Environment, University of Copenhagen, Thorvaldsensvej 40, 4000, Frederiksberg, Denmark

    J. K. Nielsen

Authors
  1. T. P. Hauser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Toneatto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. K. Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. P. Hauser.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hauser, T.P., Toneatto, F. & Nielsen, J.K. Genetic and geographic structure of an insect resistant and a susceptible type of Barbarea vulgaris in western Europe. Evol Ecol 26, 611–624 (2012). https://doi.org/10.1007/s10682-011-9515-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9515-5

Keywords

Search

Navigation