Evolutionary Ecology

, Volume 32, Issue 2–3, pp 265–285 | Cite as

Neutral and non-neutral factors shape an emergent plant–antagonist interaction

  • Rebecca F. Hazen
  • Kristine N. Moody
  • Michael J. Blum
Original Paper


Discerning the mechanisms responsible for emergent evolutionary radiations, community assembly, and the maintenance of diversity is necessary for understanding the evolutionary ecology of species interactions in changing landscapes. These processes can be driven by stochastic (neutral) factors, such as genetic drift, or deterministic (non-neutral) factors, such as the external environment and heritable phenotypic variation. Neutral and non-neutral factors can shape species interactions, but the relative influence of these different processes on antagonistic relationships is not well understood. We leveraged the recent discovery of a novel herbivore (Caloptilia triadicae) on invasive Chinese tallow (Triadica sebifera) to investigate the nature and relative importance of different factors influencing plant–antagonist interactions. We assessed measures of host attributes, herbivore demography and herbivory across the North American range of Triadica according to geography, environmental variation, and host genetic variation. We found that leaf toughness corresponded to genetic variation in Triadica, longitude, and mean temperature. Genetic variation in Triadica was the strongest predictor of herbivore abundance, especially for the early leaf mining stages, though herbivore abundance also corresponded to longitude. Model variables did not explain leaf damage, which was driven by interactions with late-stage larvae. Trends in herbivore demography were not consistent with previously reported geographic patterns of Triadica genetic variation related to tannin defense, but were consistent with patterns revealed by other studies of Triadica phenolic compounds and C:N, as well as low sensitivity of endophagous herbivores to tannins in the absence of parasitoids. Our findings suggest that even simple geographic mosaics of genetic and environmental variation, as well as distance-dependent dispersal, can influence the establishment and trajectory of novel species interactions.


Caloptilia triadicae EICA Endophagous herbivore Host genetics Isolation by distance Triadica sebifera Geographic mosaic 



Many thanks to E. Siemann, G. Wheeler, D. Davis, J. Ding, S. DeWalt, N.W. Cooper, M. Fox, E. Derryberry, A. Kawahara, S. Van Bael, J. Karubian, C. Richards-Zawacki, L.A. Dyer, S. Rifai, E.R. Haskins, V.L. Aberdeen, J.K. Davis, and several anonymous reviewers for guidance, support and input on this study. We would like to acknowledge S. Piper, M.M. Ryan, R. da Silva Nascimento, M. Dakin, B. Kravis, A.B. Uzunian, H.L. Handley, A.B. Quinlan, K.A. Hazen, J.R. Hazen, and Earthwatch volunteers for field and laboratory support. Funding for this study was provided by the National Science Foundation EAPSI program and Tulane University.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

10682_2018_9935_MOESM1_ESM.pdf (66 kb)
Supplementary material 1 (PDF 66 kb)
10682_2018_9935_MOESM2_ESM.pdf (282 kb)
Supplementary material 2 (PDF 281 kb)
10682_2018_9935_MOESM3_ESM.pdf (259 kb)
Supplementary material 3 (PDF 259 kb)
10682_2018_9935_MOESM4_ESM.pdf (367 kb)
Supplementary material 4 (PDF 366 kb)


  1. Adams JM, Zhang Y (2009) Is there more insect folivory in warmer temperate climates? A latitudinal comparison of insect folivory in eastern North America. J Ecol 97(5):933–940CrossRefGoogle Scholar
  2. Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149CrossRefPubMedGoogle Scholar
  3. Alstad D (1998) Population structure and the conundrum of local adaptation. In: Genetic structure and local adaptation in natural insect populations: effects of ecology, life history, and behavior, vol 1. Springer, US, pp 3–21Google Scholar
  4. Barber NA, Marquis RJ (2011) Leaf quality, predators, and stochastic processes in the assembly of a diverse herbivore community. Ecology 92(3):699–708CrossRefPubMedGoogle Scholar
  5. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15(4):365–377CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83(5):887–889CrossRefGoogle Scholar
  7. Body M, Kaiser W, Dubreuil G, Casas J, Giron D (2013) Leaf-miners co-opt microorganisms to enhance their nutritional environment. J Chem Ecol 39(7):969–977CrossRefPubMedGoogle Scholar
  8. Buse A, Good JEG, Dury S, Perrins CM (1998) Effects of elevated temperature and carbon dioxide on the nutritional quality of leaves of oak (Quercus robur L.) as food for the winter moth (Operophtera brumata L.). Funct Ecol 12(5):742–749CrossRefGoogle Scholar
  9. Buse A, Dury SJ, Woodburn RJW, Perrins CM, Good JEG (1999) Effects of elevated temperature on multi-species interactions: the case of Pedunculate Oak, Winter Moth and Tits. Funct Ecol 13(s1):74–82CrossRefGoogle Scholar
  10. Carmona D, Lajeunesse M, Johnson M (2010) Plant traits predict resistance to herbivores. Funct Ecol 25(2):358–367CrossRefGoogle Scholar
  11. Connor EF (2006) Effects of the light environment on oviposition preference and survival of a leaf-mining Moth, Cameraria Hamadryadella (Lepidoptera: Gracillariidae), on Quercus alba L. Ecol Entomol 31(2):179–184CrossRefGoogle Scholar
  12. Cornelissen T (2011) Climate change and its effects on terrestrial insects and herbivory patterns. Neotropical Entomol 40(2):155–163CrossRefGoogle Scholar
  13. Cornelissen T, Stiling P (2006) Does low nutritional quality act as a plant defence? An experimental test of the slow-growth, high-mortality hypothesis. Ecol Entomol 31(1):32–40CrossRefGoogle Scholar
  14. Dai-jun J, Hui-kun H (1984) The distribution of Sapium Sebiferum (Roxb) in relation to the environmental conditions. Guihaia. Accessed on July 2015
  15. Davis DR, Fox MS, Hazen RF (2013) Systematics and biology of Caloptilia Triadicae (Lepidoptera: Gracillariidae), a new species of leafmining moth of the invasive Chinese tallow tree (Triadica Sebifera (L.) Euphorbiaceae). J Lepidopterists Soc 67(4):281–290CrossRefGoogle Scholar
  16. DeLucia EH, Nabity PD, Zavala JA, Berenbaum MR (2012) Climate change: resetting plant-insect interactions. Plant Physiol 160(4):1677–1685CrossRefPubMedPubMedCentralGoogle Scholar
  17. DeWalt SJ, Siemann E, Rogers WE (2006) Microsatellite markers for an invasive tetraploid tree, Chinese tallow (Triadica sebifera). Mol Ecol Notes 6(2):505–507CrossRefGoogle Scholar
  18. DeWalt SJ, Siemann E, Rogers WE (2011) Geographic distribution of genetic variation among native and introduced populations of Chinese tallow tree, Triadica sebifera (Euphorbiaceae). Am J Bot 98(7):1128–1138CrossRefPubMedGoogle Scholar
  19. Elzinga JA, Turin H, van Damme JMM, Biere A (2005) Plant population size and isolation affect herbivory of Silene latifolia by the specialist herbivore Hadena bicruris and parasitism of the herbivore by parasitoids. Oecologia 144(3):416–426CrossRefPubMedGoogle Scholar
  20. Faeth SH, Bultman TL (1986) Interacting effects of increased tannin levels on leaf-mining insects. Entomol Exp Appl 40(3):297–301CrossRefGoogle Scholar
  21. Felker-Quinn E, Schweitzer JA, Bailey JK (2013) Meta-analysis reveals evolution in invasive plant species but little support for Evolution of Increased Competitive Ability (EICA). Ecol Evol 3(3):739–751CrossRefPubMedPubMedCentralGoogle Scholar
  22. Forkner RE, Marquis RJ, Lill JT, Corff JL (2008) Timing is everything? Phenological synchrony and population variability in leaf-chewing herbivores of Quercus. Ecol Entomol 33(2):276–285CrossRefGoogle Scholar
  23. Fox M, Hazen R, Wheeler GS, Davis DR (2012) Using internet images to gather distributional data for a newly discovered Caloptilia species (Lepidoptera: Gracillariidae) specializing on Chinese tallow in North America. Am Entomol 58(1):32–35CrossRefGoogle Scholar
  24. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  25. Han P, Lavoir A, Le Bot J, Amiens-Desneux E, Desneux N (2014) Nitrogen and water availability to tomato plants triggers bottom-up effects on the leafminer Tuta absoluta. Sci Rep 4:4455CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hazen RF (2015) The emergence and evolution of an antagonistic plant-animal Interaction. (Doctoral dissertation). Retrieved from ProQuest Dissertations and Theses (Accession Order No. 10388)Google Scholar
  27. Hazen RF, Blum MJ (2016) Host genetic variation and microenvironment shape an emergent plant–antagonist interaction. Evol Ecol 30:1–18CrossRefGoogle Scholar
  28. Hazen RF, Fox MS (2011) A cascading classroom: the benefits of utilizing teachers and students as citizen scientists in research. Am Entomol 58(1):11–14CrossRefGoogle Scholar
  29. Huang W, Siemann E, Wheeler GS, Zou J, Carrillo J, Ding J (2010) Resource allocation to defence and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J Ecol 98(5):1157–1167CrossRefGoogle Scholar
  30. Jamieson G, McKinney R (1938) Stillingia oil. J Am Oil Chem Soc 15(11):295–296Google Scholar
  31. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8(7):704–714CrossRefGoogle Scholar
  32. Kaltz O, Shykoff JA (1998) Local adaptation in host–parasite systems. Heredity 81(4):361–370CrossRefGoogle Scholar
  33. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17(4):164–170CrossRefGoogle Scholar
  34. Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11(8):852–866CrossRefPubMedGoogle Scholar
  35. Kozlov MV (2003) Density fluctuations of the leafminer Phyllonorycter strigulatella (Lepidoptera: Gracillariidae) in the impact zone of a power plant. Environ Pollut 121(1):1–10CrossRefPubMedGoogle Scholar
  36. Lee SK (1956) Genus Sapium in the Chinese flora. Acta Phytotaxon Sin 5:111–130Google Scholar
  37. Legendre P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. J Plant Ecol 1(1):3–8CrossRefGoogle Scholar
  38. Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794CrossRefGoogle Scholar
  39. Moctezuma C, Hammerbacher A, Heil M, Gershenzon J, Alonzo RM, Oyama K (2014) Specific polyphenols and tannins are associated with defense against insect herbivores in the Tropical Oak Quercus oleoides. J Chem Ecol 40(5):458–467CrossRefPubMedGoogle Scholar
  40. Mopper S (1996) Adaptive genetic structure in phytophagous insect populations. Trends Ecol Evol 11(6):235–238CrossRefPubMedGoogle Scholar
  41. Mopper S (2005) Phenology—how time creates spatial structure in endophagous insect populations. Ann Zool Fenn 42:327–333Google Scholar
  42. Mopper S, Stiling P, Landau K, Simberloff D, VanZandt P (2000) Spatiotemporal variation in leafminer population structure and adaptation to individual oak trees. Ecology 81:1577–1587CrossRefGoogle Scholar
  43. Müller-Schärer H, Schaffner U, Steinger T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19(8):417–422CrossRefPubMedGoogle Scholar
  44. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) vegan: community ecology package. R package version 2.4-1. Accessed on Dec 2017
  45. Pattison RR, Mack RN (2008) Potential distribution of the invasive tree Triadica Sebifera (Euphorbiaceae) in the United States: evaluating CLIMEX predictions with field trials. Glob Change Biol 14(4):813–826CrossRefGoogle Scholar
  46. Pattison RR, Mack RN (2009) Environmental constraints on the invasion of Triadica sebifera in the eastern U.S.: an experimental field assessment. Oecologia 158:591–602CrossRefPubMedGoogle Scholar
  47. Pearse IS, Hipp AL (2009) Phylogenetic and trait similarity to a native species predict herbivory on non-native oaks. PNAS 106(43):18097–18102CrossRefPubMedPubMedCentralGoogle Scholar
  48. Peres-Neto PR, Legendre P (2010) Estimating and controlling for spatial structure in the study of ecological communities. Glob Ecol Biogeogr 19(2):174–184CrossRefGoogle Scholar
  49. Rao CR (1964) The use and interpretation of principal component analysis in applied research. Sankhya Ser. A 26:329–359Google Scholar
  50. Renne IJ, Gauthreaux SA Jr, Gresham CA (2000) Seed dispersal of the Chinese tallow tree (Sapium sebiferum (L.) Roxb.) by birds in coastal South Carolina. Am Midl Nat 144(1):202–215CrossRefGoogle Scholar
  51. Ries L, Fletcher RJ Jr, Battin J, Sisk TD (2004) Ecological responses to habitat edges: mechanisms, models, and variability explained. Annu Rev Ecol Evol Syst 35:491–522CrossRefGoogle Scholar
  52. Rogers WE, Siemann E (2004) Invasive ecotypes tolerate herbivory more effectively than native ecotypes of the Chinese tallow tree (Sapium sebiferum). J Appl Ecol 41(3):561–570CrossRefGoogle Scholar
  53. Rogers WE, Siemann E (2005) Herbivory Tolerance and compensatory differences in native and invasive ecotypes of Chinese tallow tree (Sapium sebiferum). Plant Ecol 181:57–68CrossRefGoogle Scholar
  54. Rossi AM, Stiling P (1998) The interactions of plant clone and abiotic factors on a gall-making midge. Oecologia 116(1):170–176CrossRefPubMedGoogle Scholar
  55. Sands DPA, Brancatini VA (1991) A portable penetrometer for measuring leaf toughness in insect herbivory studies. Proc Entomol Soc Wash 93:786–788Google Scholar
  56. Sax DF, Stachowicz JJ, Brown JG, Bruno JF, Dawson MN, Gaines SD, Grosberg RK (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22(9):465–471CrossRefPubMedGoogle Scholar
  57. Scrucca L (2012) dispmod: Dispersion models. R package version 1.1. Accessed on Dec 2017
  58. Siemann E, Rogers WE (2001) Genetic differences in growth of an invasive tree species. Ecol Lett 4(6):514–518CrossRefGoogle Scholar
  59. Siemann E, Rogers WE, DeWalt SJ (2006) Rapid adaptation of insect herbivores to an invasive plant. Proc R Soc 273(1602):2763–2769CrossRefGoogle Scholar
  60. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236(4803):787–792CrossRefPubMedGoogle Scholar
  61. Speight MR, Hunter MD, Watt AD (2008) Ecology of insects: concepts and applications, 2nd edn. Wiley, LondonGoogle Scholar
  62. Stireman JO, Dyer LA, Janzen DH, Singer MS, Lill JT, Marquis RJ, Ricklefs RE, Gentry GL, Hallwachs W, Coley PD, Barone JA, Greeney HF, Connahs H, Barbosa P, Morais HC, Diniz IR (2005) Climatic unpredictability and parasitism of caterpillars: implications of global warming. PNAS 102(48):17384–17387CrossRefPubMedPubMedCentralGoogle Scholar
  63. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:S1–S14CrossRefGoogle Scholar
  64. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  65. Tu J, Zhang G, Datta K, Xu C, Yuqing H, Zhang Q, Khush GS, Datta SK (2000) Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis δ-endotoxin. Nat Biotechnol 18:1101–1104CrossRefPubMedGoogle Scholar
  66. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363CrossRefPubMedGoogle Scholar
  67. Valladares F, Gianoli E, Gómez J (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176(4):749–763CrossRefPubMedGoogle Scholar
  68. Van der Putten W, Macel M, Visser M (2010) Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc B Biol Sci 365(1549):2025–2034CrossRefGoogle Scholar
  69. Wang Y, Siemann E, Wheeler GS, Zhu L, Gu X, Ding JQ (2012) Genetic variation in anti-herbivore chemical defences in an invasive plant. J Ecol 100:894–904CrossRefGoogle Scholar
  70. Ward SM, Gaskin JF, Wilson LM (2008) Ecological genetics of plant invasion: what do we know? Invasive Plant Sci Manag 1(1):98–109CrossRefGoogle Scholar
  71. Yang Q, Carrillo J, Jin H, Shang L, Hovick SM, Nijjer S, Gabler CA, Li B, Siemann E (2013) Plant-soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. Soil Biol Biochem 65:78–85CrossRefGoogle Scholar
  72. Yarnes CT, Boecklen WJ (2005) Abiotic factors promote plant heterogeneity and influence herbivore performance and mortality in Gambel’s oak (Quercus gambeii). Entomol Exp Appl 114(2):87–95CrossRefGoogle Scholar
  73. Yarnes CT, Boecklen WJ (2006) Abiotic mosaics affect variation of plant resources and influence the performance and mortality of a leaf-miner in Gambel’s oak (Quercus gambeii, Nutt.). Ecol Res 21(1):157–163CrossRefGoogle Scholar
  74. Zhang K, Lin Y (1994) Chinese tallow. China Forestry Press, BeijingGoogle Scholar
  75. Zou J, Rogers WE, DeWalt SJ, Siemann E (2006) The effect of Chinese tallow tree (Sapium sebiferum) ecotype on soil–plant system carbon and nitrogen processes. Oecologia 150(2):272–281CrossRefPubMedGoogle Scholar
  76. Zou J, Rogers WE, Siemann E (2007) Differences in morphological and physiological traits between native and invasive populations of Sapium sebiferum. Funct Ecol 21(4):721–730CrossRefGoogle Scholar
  77. Zou J, Siemann E, Rogers WE, DeWalt SJ (2008) Decreased resistance and increased tolerance to native herbivores of the invasive plant Sapium sebiferum. Ecography 31(5):663–671CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyTulane UniversityNew OrleansUSA
  2. 2.The ByWater InstituteTulane UniversityNew OrleansUSA
  3. 3.Department of BiologyTrinity UniversitySan AntonioUSA

Personalised recommendations