Evolutionary Ecology

, Volume 25, Issue 5, pp 977–992 | Cite as

The potential of a population genomics approach to analyse geographic mosaics of plant--insect coevolution

  • Kim M. C. A. Vermeer
  • Marcel Dicke
  • Peter W. de Jong


A central issue in the evolutionary ecology of species interactions is coevolution, which involves the reciprocal selection between individuals of interacting species. Understanding the importance of coevolution in shaping species interactions requires the consideration of spatial variation in their strength. This is exactly what the, recently developed, geographic mosaic theory of coevolution addresses. Another major development in the study of population ecology is the introduction of the population genomics approach in this field of research. This approach addresses spatial processes through molecular methods. It is of particular interest that population genomics is especially applicable to natural populations of non-model species. We describe how population genomics can be used in the context of the geographic mosaic of coevolution, specifically to identify coevolutionary hot-spots, and to attribute genetic variation found at specific loci to processes of selection versus trait remixing. The proposed integration of the population genomics approach with the conceptual framework of the geographic mosaic of coevolution is illustrated with a few selected, particularly demonstrative, examples from the realm of insect--plant interactions.


Geographic mosaic of coevolution Natural resistance Plant--insect interaction Population genomics 



We are grateful to John Thompson for constructive comments on a preliminary draft of this paper, and sharing his thoughts about its topic with us. We also thank two anonymous reviewers for their helpful comments.


  1. Agrawal AF, Brodie ED, Wade MJ (2001) On indirect genetic effects in structured populations. Am Nat 158:308–323PubMedCrossRefGoogle Scholar
  2. Althoff DM, Thompson JN (1999) Comparative geographic structures of two parasitoid-host interactions. Evolution 53:818–825CrossRefGoogle Scholar
  3. Avise JC (2000) Stability, equilibrium and molecular aspects of conservation in marine species. Hydrobiologia 420:Xi–XiiGoogle Scholar
  4. Benkman CW (1999) The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. Am Nat 153:S75–S91CrossRefGoogle Scholar
  5. Benkman CW, Holimon WC, Smith JW (2001) The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55:282–294PubMedGoogle Scholar
  6. Benkman CW, Parchman TL, Favis A et al (2003) Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. Am Nat 162:182–194PubMedCrossRefGoogle Scholar
  7. Berenbaum MR, Zangerl AR (1992) Genetics of physiological and behavioral resistance to host furanocoumarins in the parsnip webworm. Evolution 46:1373–1384CrossRefGoogle Scholar
  8. Bermingham E, Avise JC (1986) Molecular zoogeography of fresh-water fishes in the southeastern United-States. Genetics 113:939–965PubMedGoogle Scholar
  9. Black WC IV, Baer CF, Antolin MF et al (2001) Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol 46:441–469PubMedCrossRefGoogle Scholar
  10. Bohonak AJ (1998) Genetic population structure of the fairy shrimp Branchinecta coloradensis (Anostraca) in the Rocky Mountains of Colorado. Can J Zool 76:2049–2057Google Scholar
  11. Brito PH, Edwards SV (2009) Multilocus phylogeography and phylogenetics using sequence-based markers. Genetica 135:439–455PubMedCrossRefGoogle Scholar
  12. Brodie ED Jr, Ridenhour BJ, Brodie ED III (2002) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082PubMedGoogle Scholar
  13. Burdon JJ, Thrall PH (1999) Spatial and temporal patterns in coevolving plant and pathogen associations. Am Nat 153:S15–S33CrossRefGoogle Scholar
  14. Butlin RK (2010) Population genomics and speciation. Genetica 138:409–418PubMedCrossRefGoogle Scholar
  15. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522PubMedCrossRefGoogle Scholar
  16. Courtney S (1988) If it’s not coevolution, it must be predation. Ecology 69:910–911CrossRefGoogle Scholar
  17. Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, LondonGoogle Scholar
  18. Darwin CR (1862) On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing. John Murray, LondonGoogle Scholar
  19. 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 266:103–111CrossRefGoogle Scholar
  20. de Jong PW, Nielsen JK (2002) Host plant use of Phyllotreta nemorum: do coadapted gene complexes play a role? Ent Exp Appl 104:207–215CrossRefGoogle Scholar
  21. de Jong PW, de Vos H, Nielsen JK (2001) Demic structure and its relation with the distribution of an adaptive trait in danish flea beetles. Mol Ecol 10:1323–1332PubMedCrossRefGoogle Scholar
  22. de Jong PW, Breuker CJ, de Vos H et al (2009) Genetic differentiation between resistance phenotypes in the phytophagous flea beetle, Phyllotreta nemorum. J Ins Sci 9:69Google Scholar
  23. Dicke M, van Loon JJA, de Jong PW (2004) Ecogenomics benefits community ecology. Science 305:618–619PubMedCrossRefGoogle Scholar
  24. Egan SP, Funk DJ (2006) Individual advantages to ecological specialization: insights on cognitive constraints from three conspecific taxa. Proc R Soc Lond B 273:843–848CrossRefGoogle Scholar
  25. Egan SP, Nosil P, Funk DJ (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62:1162–1181PubMedCrossRefGoogle Scholar
  26. Ehrlich PR, Raven PH (1964) Butterflies and plants—a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  27. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to the human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  28. Fox LR (1981) Defense and dynamics in plant-herbivore systems. Am Zool 21:853–864Google Scholar
  29. Fox LR (1988) Diffuse coevolution within complex communities. Ecology 69:906–907CrossRefGoogle Scholar
  30. Funk DJ (1998) Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52:1744–1759CrossRefGoogle Scholar
  31. Funk DJ, Nosil P (2008) Comparative analyses and ecological speciation in herbivorous insects. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 117–135Google Scholar
  32. Funk DJ, Filchak KE, Feder JL (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116:251–267PubMedCrossRefGoogle Scholar
  33. Futuyma DJ (2009) Evolution. Sinauer Associates Inc., SunderlandGoogle Scholar
  34. Futuyma DJ, Slatkin M (1983) Coevolution. Sinauer Associates Inc., SunderlandGoogle Scholar
  35. Gillet EM, Gregorius H-R (2008) Measuring differentiation among populations at different levels of genetic integration. BMC Genet 9:60PubMedCrossRefGoogle Scholar
  36. Gomez JM, Abdelaziz M, Camacho JPM et al (2009a) Local adaptation and maladaptation to pollinators in a generalist geographic mosaic. Ecol Lett 12:672–682PubMedCrossRefGoogle Scholar
  37. Gomez JM, Perfectti F, Bosch J et al (2009b) A geographic selection mosaic in a generalized plant-pollinator-herbivore system. Ecol Monogr 79:245–263CrossRefGoogle Scholar
  38. Gomulkiewicz R, Drown DM, Dybdahl MF et al (2007) Dos and don’ts of testing the geographic mosaic theory of coevolution. Heredity 98:249–258PubMedCrossRefGoogle Scholar
  39. Gregorius H-R, Degen B, König A (2007) Problems in the analysis of genetic differentiation among populations—a case study in quercus robur. Silvae Genet 56:190–199Google Scholar
  40. Hanski I (1998) Metapopulation dynamics. Nature 396:41–49CrossRefGoogle Scholar
  41. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedGoogle Scholar
  42. Herrera CM, Bazaga P (2008) Population-genomic approach reveals adaptive floral divergence in discrete populations of a hawk moth-pollinated violet. Mol Ecol 17:5378–5390PubMedCrossRefGoogle Scholar
  43. Hickerson MJ, Carstens BC, Cavender-Bares J et al (2010) Phylogeography’s past, present and future: 10 years after Avise, 2000. Mol Phylogen Evol 54:291–301CrossRefGoogle Scholar
  44. Ikeda H, Setoguchi H (2010) Natural selection on PHYE by latitude in the Japanese archipelago: insight from locus specific phylogeographic structure in Arcteria nana (Ericaceae). Mol Ecol 19:2779–2791PubMedCrossRefGoogle Scholar
  45. Iwao K, Rausher MD (1997) Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am Nat 149:316–335CrossRefGoogle Scholar
  46. Janzen DH (1980) When is it coevolution? Evolution 34:611–612CrossRefGoogle Scholar
  47. Jermy T (1984) Evolution of insect host plant relationships. Am Nat 124:609–630CrossRefGoogle Scholar
  48. Jost L (2008) Gst and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  49. Kuzina V, Ekstrøm LT, Andersen SB et al (2009) Identification of defence compounds in Barbarea vulgaris against the herbivore Phyllotreta nemorum by an eco-metabolomic approach. Plant Physiol 151:1977–1990PubMedCrossRefGoogle Scholar
  50. 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 (in press)Google Scholar
  51. Laine AL (2009) Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J Exp Bot 60:2957–2970PubMedCrossRefGoogle Scholar
  52. Lively CM (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. Am Nat 153:S34–S47CrossRefGoogle Scholar
  53. Luikart G, England PR, Tallmon D et al (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994PubMedCrossRefGoogle Scholar
  54. Manel S, Conord C, Després L (2009) Genome-scan to assess the respective role of host-plant and environmental constraints on the adaptation of a widespread insect. BMC Evol Biol 9:288PubMedCrossRefGoogle Scholar
  55. Medrano M, Herrera CM (2008) Geographical structuring of genetic diversity across the whole distribution range of Narcissus longispathus, a habitat-specialist, Mediterranean narrow endemic. Ann Bot 102:183–194PubMedCrossRefGoogle Scholar
  56. Meirmans PG, Hedrick PW (2010) Assessing population structure: Fst and related measures. Mol Ecol Res (early view)Google Scholar
  57. Minder AM, Widmer A (2008) A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Mol Ecol 17:1552–1563PubMedCrossRefGoogle Scholar
  58. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323PubMedCrossRefGoogle Scholar
  59. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, ColumbiaGoogle Scholar
  60. Neuhauser C, Andow DA, Heimpel GE et al (2003) Community genetics: expanding the synthesis of ecology and genetics. Ecology 84:545–558CrossRefGoogle Scholar
  61. Nielsen JK (1997) Variation in defences of the plant Barbarea vulgaris and in counteradaptations by the flea beetle Phyllotreta nemorum. Entomol Exp Appl 82:25–35CrossRefGoogle Scholar
  62. 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 115:265–270CrossRefGoogle Scholar
  63. Nielsen JK, Nagao T, Okabe H et al (2010) Resistance in the plant, Barbarea vulgaris, and counter-adaptations in flea beetles mediated by saponins. J Chem Ecol 36:277–285PubMedCrossRefGoogle Scholar
  64. Nosil P, Egan SP, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: “Isolation by adaptation” and multiple roles for divergent selection. Evolution 62:316–336PubMedCrossRefGoogle Scholar
  65. Nuismer SL, Thompson JN (2006) Coevolutionary alternation in antagonistic interactions. Evolution 60:2207–2217PubMedGoogle Scholar
  66. Nuismer SL, Gomulkiewicz R, Morgan MT (2003) Coevolution in temporally variable environments. Am Nat 162:195–204PubMedCrossRefGoogle Scholar
  67. Orr HA (2005) The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119–127PubMedCrossRefGoogle Scholar
  68. Pellmyr O (2003) Yuccas, yucca moths, and coevolution: a review. Ann Missi Botl Gard 90:35–55CrossRefGoogle Scholar
  69. Rausher MD (1988) Is coevolution dead? Ecology 69:898–901CrossRefGoogle Scholar
  70. Rausher MD (1996) Genetic analysis of coevolution between plants and their natural enemies. Tr Genet 12:212–217CrossRefGoogle Scholar
  71. Rogers SM, Bernatchez L (2005) Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Mol Ecol 14:351–361PubMedCrossRefGoogle Scholar
  72. Schlotterer C (2002) Towards a molecular characterization of adaptation in local populations. Curr Op Genet Dev 12:683–687PubMedCrossRefGoogle Scholar
  73. Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically mediated coevolution—multiple functions for seaweed secondary metabolites. Ecology 76:107–123CrossRefGoogle Scholar
  74. Schneider CJ (2008) Exploiting genomic resources in studies of speciation and adaptive radiation of lizards in the genus Anolis. Integr Comp Biol 48:520–526PubMedCrossRefGoogle Scholar
  75. Schoonhoven LM (2005) Insect--plant relationships: the whole is more than the sum of its parts. Entomol Exp Appl 115:5–6CrossRefGoogle Scholar
  76. Schoonhoven LM, van Loon JJA, Dicke ME (2005) Insect--plant biology. Oxford University Press, OxfordGoogle Scholar
  77. Sefc KM, Payne RB, Sorensen MD (2007) Genetic differentiation after founder events: an evaluation of Fst estimators with empirical and simulated data. Evol Ecol Res 9:21–39Google Scholar
  78. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle Scholar
  79. Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135:367–374PubMedGoogle Scholar
  80. Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity 100:158–170PubMedCrossRefGoogle Scholar
  81. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688PubMedCrossRefGoogle Scholar
  82. Strong DR, Lawton JH, Southwood R (1984) Insects on plants: community patterns and mechanisms. Blackwell, OxfordGoogle Scholar
  83. Thompson JN (1988) Coevolution and alternative hypotheses on insect plant interactions. Ecology 69:893–895CrossRefGoogle Scholar
  84. Thompson JN (1994) The coevolutionary process. Univ of Chicago Press, ChicagoGoogle Scholar
  85. Thompson JN (1999a) The evolution of species interactions. Science 284:2116–2118PubMedCrossRefGoogle Scholar
  86. Thompson JN (1999b) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:S1–S14CrossRefGoogle Scholar
  87. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  88. Thompson JN (2009a) The coevolving web of life. Am Nat 173:125–140PubMedCrossRefGoogle Scholar
  89. Thompson JN (2009b) Which ecologically important traits are most likely to evolve rapidly? Oikos 118:1281–1283CrossRefGoogle Scholar
  90. Thompson JN, Pellmyr O (1992) Mutualism with pollinating seed parasites amid co-pollinators—constraints on specialization. Ecology 73:1780–1791CrossRefGoogle Scholar
  91. Thompson JN, Cunningham BM, Seagraves KA et al (1997) Plant polyploidy and insect/plant interactions. Am Nat 150:730–743PubMedCrossRefGoogle Scholar
  92. Toju H, Sota T (2006) Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection. Am Nat 167:105–117PubMedCrossRefGoogle Scholar
  93. Toneatto F, Nielsen JK, Ørgaard M et al (2010) Genetic and sexual separation between insect resistant and susceptible Barbarea vulgaris plants in Denmark. Mol Ecol 19:3456–3465PubMedCrossRefGoogle Scholar
  94. Vasemagi A, Primmer CR (2005) Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol Ecol 14:3623–3642PubMedCrossRefGoogle Scholar
  95. Verbaarschot P, Calvo D, Esselink GD et al (2007) Isolation of polymorphic microsatellite loci from the flea beetle Phyllotreta nemorum L. (Coleoptera: Chrysomelidae). Mol Ecol Notes 7:60–62CrossRefGoogle Scholar
  96. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population substructure. Evolution 38:1358–1370CrossRefGoogle Scholar
  97. Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354CrossRefGoogle Scholar
  98. Wright S (1968) Evolution and the genetics of populations: a treatise in four volumes. University of Chicago Press, ChicagoGoogle Scholar
  99. Xu H, Sarkar B, George V (2009) A new measure of population structure using multiple single nucleotide polymorphisms and its relationship with Fst. BMC Res Notes 2:21PubMedCrossRefGoogle Scholar
  100. Zangerl AR, Berenbaum MR (2003) Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57:806–815PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Kim M. C. A. Vermeer
    • 1
  • Marcel Dicke
    • 1
  • Peter W. de Jong
    • 1
  1. 1.Laboratory of EntomologyWageningen UniversityWageningenThe Netherlands

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