, Volume 178, Issue 3, pp 747–759 | Cite as

Ecological effects of aphid abundance, genotypic variation, and contemporary evolution on plants

Population ecology - Original research


Genetic variation and contemporary evolution within populations can shape the strength and nature of species interactions, but the relative importance of these forces compared to other ecological factors is unclear. We conducted a field experiment testing the effects of genotypic variation, abundance, and presence/absence of green peach aphids (Myzus persicae) on the growth, leaf nitrogen, and carbon of two plant species (Brassica napus and Solanum nigrum). Aphid genotype affected B. napus but not S. nigrum biomass explaining 20 and 7 % of the total variation, respectively. Averaging across both plant species, the presence/absence of aphids had a 1.6× larger effect size (Cohen’s d) than aphid genotype, and aphid abundance had the strongest negative effects on plant biomass explaining 29 % of the total variation. On B. napus, aphid genotypes had different effects on leaf nitrogen depending on their abundance. Aphids did not influence leaf nitrogen in S. nigrum nor leaf carbon in either species. We conducted a second experiment in the field to test whether contemporary evolution could affect plant performance. Aphid populations evolved in as little as five generations, but the rate and direction of this evolution did not consistently vary between plant species. On one host species (B. napus), faster evolving populations had greater negative effects on host plant biomass, with aphid evolutionary rate explaining 23 % of the variation in host plant biomass. Together, these results show that genetic variation and evolution in an insect herbivore can play important roles in shaping host plant ecology.


Community genetics Eco-evolutionary dynamics Herbivory Plant-herbivore Plant–insect interactions Rapid evolution 

Supplementary material

442_2015_3276_MOESM1_ESM.doc (384 kb)
Supplementary material 1 (DOC 384 kb)


  1. Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105CrossRefGoogle Scholar
  2. Agashe D (2009) The stabilizing effect of intraspecific genetic variation on population dynamics in novel and ancestral habitats. Am Nat 174:255–267. doi:10.1086/600085 PubMedCrossRefGoogle Scholar
  3. Agrawal AA (2000) Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:500–508CrossRefGoogle Scholar
  4. Agrawal AA, Underwood N, Stinchcombe JR (2004) Intraspecific variation in the strength of density dependence in aphid populations. Ecol Entomol 29:521–526CrossRefGoogle Scholar
  5. Agrawal AA, Hastings AP, Johnson MTJ et al (2012) Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113–116. doi:10.1126/science.1225977 PubMedCrossRefGoogle Scholar
  6. Antonovics J (1976) The input from population genetics: “the new ecological genetics”. Syst Bot 1:233–245CrossRefGoogle Scholar
  7. Bailey JK, Schweitzer JA, Ubeda F et al (2009) From genes to ecosystems: a synthesis of the effects of plant genetic factors across levels of organization. Philos Trans R Soc Lond B 364:1607–1616. doi:10.1098/rstb.2008.0336 CrossRefGoogle Scholar
  8. Bassar RD, Marshall MC, Lopez-Sepulcre A et al (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Natl Acad Sci USA 107:3616–3621. doi:10.1073/pnas.0908023107 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Blackman RL, Eastop VF (2008) Aphids on the world’s herbaceous plants and shrubs. Wiley, ChichesterGoogle Scholar
  10. Bohannan B, Lenski RE (2000) Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol Lett 3:362–377CrossRefGoogle Scholar
  11. Bolnick DI, Svanbäck R, Fordyce JA et al (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi:10.1086/343878 PubMedCrossRefGoogle Scholar
  12. Bone E, Farres A (2001) Trends and rates of microevolution in plants. Genetica 112:165–182PubMedCrossRefGoogle Scholar
  13. Brues CT (1924) The specificity of food-plants in the evolution of phytophagous insects. Am Nat 58:127–144CrossRefGoogle Scholar
  14. Carriére Y, Crowder DW, Tabashnik BE (2010) Evolutionary ecology of insect adaptation to Bt crops. Evol Appl 3:561–573. doi:10.1111/j.1752-4571.2010.00129.x PubMedCentralPubMedCrossRefGoogle Scholar
  15. Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum, HillsdaleGoogle Scholar
  16. Cole RA (1997) The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated Brassica species. Entomol Exp Appl 85:121–133CrossRefGoogle Scholar
  17. Devonshire AL, Field LM, Foster SP et al (1998) The evolution of insecticide resistance in the peach-potato aphid, Myzus persicae. Philos Trans R Soc Lond B 353:1677–1684. doi:10.1098/rstb.1998.0318 CrossRefGoogle Scholar
  18. Dyer KF (1964) Evolution observed—some examples of evolution occurring in historical. J Biol Educ 1–25Google Scholar
  19. Edmonds JM, Chweya JA (1997) Black Nightshades, Solanum nigrum L. and related species. Institute of Plant Genetics and Crop Plant Research, RomeGoogle Scholar
  20. Edmunds GF, Alstad DN (1978) Coevolution in insect herbivores and conifers. Science 199:941–945PubMedCrossRefGoogle Scholar
  21. Edwards OR (2001) Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts. Entomol Exp Appl 100:21–30. doi:10.1046/j.1570-7458.2001.00844.x CrossRefGoogle Scholar
  22. Emden H, Eastop VF, Hughes RD, Way MJ (1969) The ecology of Myzus persicae. Annu Rev Entomol 14:197–270CrossRefGoogle Scholar
  23. Eskin NAM, Mcdonald BE (1991) Canola oil. Nutr Bull 16:138–146. doi:10.1111/j.1467-3010.1991.tb01048.x CrossRefGoogle Scholar
  24. Farkas TE, Mononen T, Comeault AA et al (2013) Evolution of camouflage drives rapid ecological change in an insect community. Curr Biol 23:1835–1843. doi:10.1016/j.cub.2013.07.067 PubMedCrossRefGoogle Scholar
  25. Fenton B, Margaritopoulos JT, Malloch GL, Foster SP (2010) Micro-evolutionary change in relation to insecticide resistance in the peach-potato aphid, Myzus persicae. Ecol Entomol 35:131–146CrossRefGoogle Scholar
  26. Foster JE, Ohm HW, Patterson FL, Taylor PL (1991) Effectiveness of deploying single gene resistances in wheat for controlling damage by the hessian fly (Diptera: Cecidomyiidae). Environ Entomol 20:964–969CrossRefGoogle Scholar
  27. Foster SP, Denholm I, Devonshire AL (2000) The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Protect 19:873–879. doi:10.1016/S0261-2194(00)00115-0 CrossRefGoogle Scholar
  28. Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
  29. Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  30. Fry JD (1990) Trade-offs in fitness on different hosts—evidence from a selection experiment with a phytophagous mite. Am Nat 136:569–580CrossRefGoogle Scholar
  31. Fussmann GF, Loreau M, Abrams PA (2007) Eco-evolutionary dynamics of communities and ecosystems. Funct Ecol 21:465–477. doi:10.1111/j.1365-2435.2007.01275.x CrossRefGoogle Scholar
  32. Gould F (1979) Rapid host range evolution in a population of the phytophagous mite Tetranychus urticae Koch. Evolution 33:791–802Google Scholar
  33. Gould F (1983) Genetics of plant–herbivore interactions. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic, New York, pp 1–55Google Scholar
  34. Gould F (1991) The evolutionary potential of crop pests. Am Sci 496–507Google Scholar
  35. Hairston NG Jr, Ellner SP, Geber MA et al (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127. doi:10.1111/j.1461-0248.2005.00812.x CrossRefGoogle Scholar
  36. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  37. Hersch-Green EI, Turley NE, Johnson MTJ (2011) Community genetics: what have we accomplished and where should we be going? Philos Trans R Soc Lond B 366:1453–1460. doi:10.1098/rstb.2010.0331 CrossRefGoogle Scholar
  38. 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. doi:10.2307/3450841?ref=search-gateway:cffd26a81676b216725bdea740155185 CrossRefGoogle Scholar
  39. Johnson MTJ, Vellend M, Stinchcombe JR (2009) Evolution in plant populations as a driver of ecological changes in arthropod communities. Philos Trans R Soc Lond B 364:1593–1605. doi:10.1098/rstb.2008.0334 CrossRefGoogle Scholar
  40. Kant MR, Sabelis MW, Haring MA, Schuurink RC (2008) Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc R Soc Lond B 275:443–452. doi:10.1098/rspb.2007.1277 CrossRefGoogle Scholar
  41. Karban R (1989) Fine-scale adaptation of herbivorous thrips to individual host plants. Nature 340:60–61CrossRefGoogle Scholar
  42. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  43. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328. doi:10.1146/annurev.arplant.53.100301.135207 PubMedCrossRefGoogle Scholar
  44. Kinnison MT, Hendry AP (2001) The pace of modern life II: from rates of contemporary microevolution to pattern and process. Genetica 112:145–164PubMedCrossRefGoogle Scholar
  45. Loxdale HD (2010) Rapid genetic changes in natural insect populations. Ecol Entomol 35:155–164. doi:10.1111/j.1365-2311.2009.01141.x CrossRefGoogle Scholar
  46. 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
  47. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Lond B 273:2575–2584. doi:10.1073/pnas.94.4.1252 CrossRefGoogle Scholar
  48. Meihls LN, Higdon ML, Siegfried BD et al (2008) Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection. Proc Natl Acad Sci USA 105:19177–19182PubMedCentralPubMedCrossRefGoogle Scholar
  49. Meyer JR, Ellner SP, Hairston NG et al (2006) Prey evolution on the time scale of predator–prey dynamics revealed by allele-specific quantitative PCR. Proc Natl Acad Sci USA 103:10690–10695PubMedCentralPubMedCrossRefGoogle Scholar
  50. Miles PW (2007) Aphid saliva. Biol Rev 74:41–85. doi:10.1111/j.1469-185X.1999.tb00181.x CrossRefGoogle Scholar
  51. Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends Ecol Evol 11:235–238PubMedCrossRefGoogle Scholar
  52. Normark BB, Johnson NA (2011) Niche explosion. Genetica 139:551–564PubMedCrossRefGoogle Scholar
  53. Nosil P, Crespi BJ, Sandoval CP (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:440–443. doi:10.1038/417440a PubMedCrossRefGoogle Scholar
  54. Painter RH (1931) Resistance of varieties of winter wheat to Hessian fly, Phytophaga destructor. Kansas Agric Exp Stn Bull 27:1–58Google Scholar
  55. Pathak PK, Heinrichs EA (1982) Selection of biotype populations 2 and 3 of Nilaparvata lugens by exposure to resistant rice varieties. Environ Entomol 11:85–90CrossRefGoogle Scholar
  56. Pathak MD, Painter RH (1959) Geographical distribution of the four biotypes of corn leaf aphid, Rhopalosiphum maidis (Fitch) in Kansas. Trans Kansas Acad Sci 62:1. doi:10.2307/3626498 CrossRefGoogle Scholar
  57. Pimentel D (1968) Population regulation and genetic feedback. Science 159:1432–1437PubMedCrossRefGoogle Scholar
  58. Post DM, Palkovacs EP (2009) Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play. Philos Trans R Soc Lond B 364:1629–1640. doi:10.1098/rstb.2009.0012 CrossRefGoogle Scholar
  59. Post DM, Palkovacs EP, Schielke EG, Dodson SI (2008) Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology 89:2019–2032PubMedCrossRefGoogle Scholar
  60. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
  61. Rainey PB, Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394:69–72PubMedCrossRefGoogle Scholar
  62. Rakow G, Woods DL (1987) Outcrossing in rape and mustard under Saskatchewan prairie conditions. Can J Plant Sci 67:147–151. doi:10.4141/cjps87-017 CrossRefGoogle Scholar
  63. Rausher MD (2001) Co-evolution and plant resistance to natural enemies. Nature 411:857–864. doi:10.1038/35081193 PubMedCrossRefGoogle Scholar
  64. Rodriguez-Saona CR, Musser RO, Vogel H et al (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057. doi:10.1007/s10886-010-9854-7 PubMedCrossRefGoogle Scholar
  65. Schmidt DD, Kessler A, Kessler D et al (2004) Solanum nigrum: a model ecological expression system and its tools. Mol Ecol 13:981–995. doi:10.1111/j.1365-294X.2004.02111.x PubMedCrossRefGoogle Scholar
  66. Schulte RD, Makus C, Hasert B et al (2010) Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc Natl Acad Sci USA 107:7359–7364. doi:10.1073/pnas.1003113107 PubMedCentralPubMedCrossRefGoogle Scholar
  67. Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect–host associations. Nature 366:681–683CrossRefGoogle Scholar
  68. Sloane MA, Sunnucks P, Wilson AC, Hales DF (2001) Microsatellite isolation, linkage group identification and determination of recombination frequency in the peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Genet Res 77:251–260PubMedCrossRefGoogle Scholar
  69. Soria-Carrasco V, Gompert Z, Comeault AA et al (2014) Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344:738–742. doi:10.1126/science.1252136 PubMedCrossRefGoogle Scholar
  70. Strauss SY (1997) Lack of evidence for local adaptation to individual plant clones or site by a mobile specialist herbivore. Oecologia 110:77–85CrossRefGoogle Scholar
  71. Tabashnik BE, Van Rensburg JBJ, Carriére Y (2009) Field-evolved insect resistance to Bt crops: definition, theory, and data. J Econ Entomol 102:2011–2025PubMedCrossRefGoogle Scholar
  72. Tack AJM, Roslin T (2010) Overrun by the neighbors: landscape context affects strength and sign of local adaptation. Ecology 91:2253–2260PubMedCrossRefGoogle Scholar
  73. Tetard-Jones C, Kertesz MA, Gallois P, Preziosi RF (2007) Genotype-by-genotype interactions modified by a third species in a plant–insect system. Am Nat 170:492–499. doi:10.1086/520115 PubMedCrossRefGoogle Scholar
  74. Thompson JN (1998) Rapid evolution as an ecological process. Trends Ecol Evol 13:329–332PubMedCrossRefGoogle Scholar
  75. Thompson JN (2013) Relentless evolution. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  76. Turcotte MM, Reznick DN, Hare JD (2011) The impact of rapid evolution on population dynamics in the wild: experimental test of eco-evolutionary dynamics. Ecol Lett 14:1084–1092. doi:10.1111/j.1461-0248.2011.01676.x PubMedCrossRefGoogle Scholar
  77. Underwood N, Rausher MD (2000) The effects of host–plant genotype on herbivore population dynamics. Ecology 81:1565–1576CrossRefGoogle Scholar
  78. Utsumi S (2011) Eco-evolutionary dynamics in herbivorous insect communities mediated by induced plant responses. Popul Ecol 53:23–34. doi:10.1007/s10144-010-0253-2 CrossRefGoogle Scholar
  79. Van Zandt PA, Mopper S (1998) A meta-analysis of adaptive deme formation in phytophagous insect populations. Am Nat 152:595–604. doi:10.1086/286192 PubMedCrossRefGoogle Scholar
  80. Via S (1990) Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. Annu Rev Entomol 35:421–446. doi:10.1146/annurev.en.35.010190.002225 PubMedCrossRefGoogle Scholar
  81. Viswanathan DV, Narwani AJ, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896CrossRefGoogle Scholar
  82. von Burg S, Ferrari J, Muller CB, Vorburger C (2008) Genetic variation and covariation of susceptibility to parasitoids in the aphid Myzus persicae: no evidence for trade-offs. Proc R Soc Lond B 275:1089–1094. doi:10.1126/science.1094611 CrossRefGoogle Scholar
  83. Vorburger C (2006) Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae. J Evol Biol 19:97–107. doi:10.1111/j.1420-9101.2005.00985.x PubMedCrossRefGoogle Scholar
  84. Vorburger C, Sunnucks P, Ward SA (2003) Explaining the coexistence of asexuals with their sexual progenitors: no evidence for general-purpose genotypes in obligate parthenogens of the peach-potato aphid, Myzus persicae. Ecol Lett 6:1091–1098. doi:10.1046/j.1461-0248.2003.00536.x CrossRefGoogle Scholar
  85. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216. doi:10.1007/s003440000026 PubMedGoogle Scholar
  86. Wasserman SS, Futuyma DJ (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil, Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae). Evolution 605–617Google Scholar
  87. Weber G (1986) Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae. Entomol Exp Appl 40:161–168CrossRefGoogle Scholar
  88. Whitham TG, Young WP, Martinsen GD et al (2003) Community and ecosystem genetics: a consequence of the extended phenotype. Ecology 84:559–573. doi:10.2307/3107845?ref=search-gateway:bb6c26f53ae3213567b80e08cf30c839 CrossRefGoogle Scholar
  89. Wilson AC, Massonnet B, Simon JC et al (2004) Cross-species amplification of microsatellite loci in aphids: assessment and application. Mol Ecol Notes 4:104–109. doi:10.1046/j.1471-8286.2003.00584.x CrossRefGoogle Scholar
  90. Wimp GM, Martinsen GD, Floate KD et al (2005) Plant genetic determinants of arthropod community structure and diversity. Evolution 59:61–69. doi:10.1111/j.0014-3820.2005.tb00894.x PubMedCrossRefGoogle Scholar
  91. Yoshida T, Ellner SP, Jones LE et al (2007) Cryptic population dynamics: rapid evolution masks trophic interactions. PLoS Biol 5:e235. doi:10.1371/journal.pbio.0050235.sd002 PubMedCentralPubMedCrossRefGoogle Scholar
  92. Zust T, Heichinger C, Grossniklaus U et al (2012) Natural enemies drive geographic variation in plant defenses. Science 338:116–119. doi:10.1126/science.1226397 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of BiologyUniversity of Toronto MississaugaMississaugaCanada
  2. 2.Department of Plant BiologyMichigan State UniversityEast LansingUSA

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