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Enhanced survival of a specialized leaf beetle reveals potential trade-offs with host utilization traits

  • Carlos Bustos-SeguraEmail author
  • Daniel González-Tokman
  • Juan Fornoni
Original Paper

Abstract

The most evident trade-off in specialized herbivores is the reduction of host range. However, trade-offs that limit the adaptation of specialized herbivores to an evolving host could exist and have been scarcely explored. Here, we tested whether the specialized leaf beetle species Lema daturaphila expresses trade-offs related to its co-adaptation with the host plant species Datura stramonium. Firstly, we found that increases in the concentration of scopolamine, a tropane alkaloid that is produced by the plant species, reduce beetle survival, showing that scopolamine is still a defensive trait against the specialized herbivores. In addition, we performed a selection experiment to increase survival of the beetles on the normal host and explored the consequences for life history and host-related traits and the corresponding G-matrix. After three selection events, we observed an improvement of survival in the selection line, but no correlational selection on other traits. There was also evidence that the G-matrix structure changed after selection. The genetic correlations between fecundity and relative growth rate and consumption efficiency were negative in the selection line, but neutral in the control line. The change in genetic correlations after selection suggests that there are trade-offs between survival and host utilization traits, which have the potential to limit the beetles’ co-adaptation to evolving plant defenses.

Keywords

Trade-offs Alkaloids Fitness cost Life history evolution Chrysomelidae Rapid evolution Pleiotropy 

Notes

Acknowledgements

Thanks to Luz Lamas, Ileana Mondragon and Dalia Ponce for assistance during the experimental work. Yesenia Villalobos performed lipid extractions. We thank Constantino Macias and Jaime Zuñiga for helpful discussions throughout the study, and Lynna Kiere for providing useful comments on the manuscript. CBS was supported by a CONACYT postgraduate scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Agrawal AA (2000) Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. Ecology 81:500–508CrossRefGoogle Scholar
  2. Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. Evol Darwin 150:243–268Google Scholar
  3. Alexander J, Benford D, Cockburn A, Cravedi J, Dogliotti E, Domenico A, Di et al (2008) Scientific opinion of the panel on contaminants in the food chain on a request from the european commission on tropane alkaloids (from Datura sp.) as undesirable substances in animal feed. EFSA J 691:1–55Google Scholar
  4. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302CrossRefGoogle Scholar
  5. Arnold SJ, Bürger R, Hohenlohe PA, Ajie BC, Jones AG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62:2451–2461CrossRefGoogle Scholar
  6. Becerra JX (1994) Squirt-Gun defense in Bursera and the chrysomelid counterploy. Ecology 75:1991–1996CrossRefGoogle Scholar
  7. Bégin M, Roff DA (2001) An analysis of G matrix variation in two closely related cricket species Gryllus firmus and G pennsylvanicus. J Evol Biol 14:1–13CrossRefGoogle Scholar
  8. Berenbaum MR (1978) Toxicity of a furanocoumarin to armyworms: a case of biosynthetic escape from insect herbivores. Science 201:532–534CrossRefGoogle Scholar
  9. Berenbaum MR, Feeny P (1981) Toxicity of angular furanocoumarins to swallowtail butterflies: escalation in a coevolutionary arms race? Science 212:927–929CrossRefGoogle Scholar
  10. Brévault T, Heuberger S, Zhang M, Ellers-Kirk C, Ni X, Masson L et al (2013) Potential shortfall of pyramided transgenic cotton for insect resistance management. Proc Natl Acad Sci USA 110:5806–5811CrossRefGoogle Scholar
  11. Bustos-Segura C, Fornoni J, Núñez-Farfán J (2014) Evolutionary changes in plant tolerance against herbivory through a resurrection experiment. J Evol Biol 27:488–496CrossRefGoogle Scholar
  12. Calsbeek B, Goodnight CJ (2009) Empirical comparison of G matrix test statistics: finding biologically relevant change. Evolution 63:2627–2635CrossRefGoogle Scholar
  13. Carriére Y, Ellers-Kirk C, Liu Y-B, Sims MA, Patin AL, Dennehy TJ et al (2001) Fitness costs and maternal effects associated with resistance to transgenic cotton in the pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 94:1571–1576CrossRefGoogle Scholar
  14. Castillo G, Cruz LL, Tapia-López R, Olmedo-Vicente E, Carmona D, Anaya-Lang AL et al (2014) Selection mosaic exerted by specialist and generalist herbivores on chemical and physical defense of Datura stramonium. PLoS ONE 9:e102478CrossRefGoogle Scholar
  15. Castillo G, Valverde PL, Cruz LL, Hernández-Cumplido J, Andraca-Gómez G, Fornoni J et al (2015) Adaptive divergence in resistance to herbivores in Datura stramonium. PeerJ 3:e1411CrossRefGoogle Scholar
  16. Collet JM, Fuentes S, Hesketh J, Hill MS, Innocenti P, Morrow EH et al (2016) Rapid evolution of the intersexual genetic correlation for fitness in Drosophila melanogaster. Evolution 70:781–795CrossRefGoogle Scholar
  17. Córdoba-Aguilar A, Nava-Sánchez A, González-Tokman DM, Munguía-Steyer R, Gutiérrez-Cabrera AE (2016) Immune priming fat reserves muscle mass and body weight of the house cricket is affected by diet composition. Neotrop Entomol 45:404–410CrossRefGoogle Scholar
  18. Cornell HV, Hawkins BA (2003) Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am Nat 161:507–522CrossRefGoogle Scholar
  19. Crawley MJ (2005) Statistics: an introduction using R. Wiley, HobokenCrossRefGoogle Scholar
  20. Cullingham CI, Cooke JEK, Dang S, Davis CS, Cooke BJ, Coltman DW (2011) Mountain pine beetle host-range expansion threatens the boreal forest. Mol Ecol 20:2157–2171CrossRefGoogle Scholar
  21. Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbic M et al (2013) A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Natl Acad Sci USA 110:E113–E122CrossRefGoogle Scholar
  22. Després L, David J-P, Gallet C (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol 22:298–307CrossRefGoogle Scholar
  23. Doroszuk A, Wojewodzic MW, Gort G, Kammenga JE (2008) Rapid divergence of genetic variance-covariance matrix within a natural population. Am Nat 171:291–304CrossRefGoogle Scholar
  24. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  25. Espinosa EG, Fornoni J (2006) Host tolerance does not impose selection on natural enemies. New Phytol 170:609–614CrossRefGoogle Scholar
  26. Fordyce JA (2010) Host shifts and evolutionary radiations of butterflies. Proc Biol Sci 277:3735–3743CrossRefGoogle Scholar
  27. Forister ML, Ehmer AG, Futuyma DJ (2007) The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle. J Evol Biol 20:985–996CrossRefGoogle Scholar
  28. Fornoni J, Núñez-Farfán J (2000) Evolutionary ecology of Datura stramonium: genetic variation and costs for tolerance to defoliation. Evolution 54:789–797CrossRefGoogle Scholar
  29. Fornoni J, Valverde PL, Núñez-Farfán J (2003) Quantitative genetics of plant tolerance and resistance against natural enemies in two natural populations of Datura stramonium. Evol Ecol Res 5:1049–1065Google Scholar
  30. Frago E, Bauce E (2014) Life-history consequences of chronic nutritional stress in an outbreaking insect defoliator. PLoS ONE 9:e88039CrossRefGoogle Scholar
  31. 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
  32. Fukano Y, Doi H, Thomas CE, Takata M, Koyama S, Satoh T (2016) Contemporary evolution of host plant range expansion in an introduced herbivorous beetle Ophraella communa. J Evol Biol 29:757–765CrossRefGoogle Scholar
  33. Garrido E, Andraca-Gómez G, Fornoni J (2012) Local adaptation: simultaneously considering herbivores and their host plants. New Phytol 193:445–453CrossRefGoogle Scholar
  34. Gassmann AJ, Onstad DW, Pittendrigh BR (2009) Evolutionary analysis of herbivorous insects in natural and agricultural environments. Pest Mangem Sci 65:1174–1181CrossRefGoogle Scholar
  35. Gompert Z, Messina FJ (2016) Genomic evidence that resource-based trade-offs limit host-range expansion in a seed beetle. Evolution 70:1249–1264CrossRefGoogle Scholar
  36. Groeters FR, Tabashnik BE, Finson N, Johnson MW (1994) Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution 48:197–201Google Scholar
  37. Hughes RA (1982) Anticholinergic drugs blood-brain-barrier and tonic immobility in chickens. Physiol Behav 29:67–71CrossRefGoogle Scholar
  38. Joussen N, Agnolet S, Lorenz S, Schone SE, Ellinger R, Schneider B et al (2012) Resistance of Australian Helicoverpa armigera to fenvalerate is due to the chimeric P450 enzyme CYP337B3. Proc Natl Acad Sci USA 109:15206–15211CrossRefGoogle Scholar
  39. Kalra B, Parkash R (2014) Trade-off of ovarian lipids and total body lipids for fecundity and starvation resistance in tropical populations of Drosophila melanogaster. J Evol Biol 27:2371–2385CrossRefGoogle Scholar
  40. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J, Schimmel BCJ et al (2015) Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann Bot 115:1015–1051CrossRefGoogle Scholar
  41. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC (2012) Experimental evolution. Trends Ecol Evol 27:547–560CrossRefGoogle Scholar
  42. Kergoat GJ, Delobel A, Fédière G, Rü B, Le, Silvain J-F (2005) Both host-plant phylogeny and chemistry have shaped the African seed-beetle radiation. Mol Phylogenet Evol 35:602–611CrossRefGoogle Scholar
  43. Kingsolver JG, Shlichta JG, Ragland GJ, Massie KR (2006) Thermal reaction norms for caterpillar growth depend on diet. Evol Ecol Res 8:703–715Google Scholar
  44. Kogan M, Goeden RD (1970) The biology of Lema trilineata daturaphila (Coleoptera: Chrysomelidae) with notes on efficiency of food utilization by larvae. Ann Entomol Soc Am 63:537–546CrossRefGoogle Scholar
  45. Kogan M, Goeden RD (1971) Feeding and host-selection behavior of Lema trilineata daturaphila larvae (Coleoptera: Chrysomelidae). Ann Entomol Soc Am 64:1435–1448CrossRefGoogle Scholar
  46. Krug E, Proksch P (1993) Influence of dietary alkaloids on survival and growth of Spodoptera littoralis. Biochem Syst Ecol 21:749–756CrossRefGoogle Scholar
  47. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philos Trans R Soc London B 359:873–890CrossRefGoogle Scholar
  48. Lee KP, Raubenheimer D, Simpson SJ (2004) The effects of nutritional imbalance on compensatory feeding for cellulose-mediated dietary dilution in a generalist caterpillar. Physiol Entomol 29:108–117CrossRefGoogle Scholar
  49. Leroi AM, Chippindale AK, Rose MR (1994) Long-term laboratory evolution of a genetic life-history trade-off in Drosophila melanogaster 1. The role of genotype-by-environment interaction. Evolution 48:1244–1257Google Scholar
  50. Maubecin C, Cosacov A, Sersic A, Fornoni J, Benítez-Vieyra S (2016) Drift effects on the multivariate floral phenotype of Calceolaria polyrhiza during a postglacial expansion in Patagonia. J Evol Biol 29:1523–1534CrossRefGoogle Scholar
  51. Messina FJ, Durham SL (2015) Loss of adaptation following reversion suggests trade-offs in host use by a seed beetle. J Evol Biol 28:1882–1891CrossRefGoogle Scholar
  52. Núñez-Farfán J, Dirzo R (1994) Evolutionary ecology of Datura stramonium L In Central Mexico: natural selection for resistance to herbivorous insects. Evolution 48:423–436CrossRefGoogle Scholar
  53. Pavličev M, Cheverud JM (2015) Constraints evolve: context dependency of gene effects allows evolution of pleiotropy. Annu Rev Ecol Evol Syst 46:413–434CrossRefGoogle Scholar
  54. Petschenka G, Agrawal AA (2016) How herbivores coopt plant defenses: natural selection specialization and sequestration. Curr Opin Insect Sci 14:17–24CrossRefGoogle Scholar
  55. Phillips PC, Arnold SJ (1999) Hierarchical comparison of genetic variance-covariance matrices I using the Flury hierarchy. Evolution 53:1506–1515CrossRefGoogle Scholar
  56. Roff DA (2002) Comparing G matrices: a MANOVA approach. Evolution 56:1286–1291CrossRefGoogle Scholar
  57. Roff DA, Fairbairn D (2012) The evolution of trade-offs under directional and correlational selection. Evolution 66:2461–2474CrossRefGoogle Scholar
  58. Roff DA, Mostowy S, Fairbairn DJ (2002) The evolution of trade-offs: testing predictions on response to selection and environmental variation. Evolution 56:84–95CrossRefGoogle Scholar
  59. Roff DA, Prokkola JM, Krams I, Rantala MJ (2012) There is more than one way to skin a G matrix. J Evol Biol 25:1113–1126CrossRefGoogle Scholar
  60. Schuman MC, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61:373–394CrossRefGoogle Scholar
  61. Scott JG, Liu N, Wen Z (1998) Insect cytochromes P450: diversity insecticide resistance and tolerance to plant toxins. Comp Biochem Physiol C 121:147–155Google Scholar
  62. Sgro C, Hoffmann A (2004) Genetic correlations tradeoffs and environmental variation. Heredity 93:241–248CrossRefGoogle Scholar
  63. Shonle I, Bergelson J (2000) Evolutionary ecology of the tropane alkaloids of Datura stramonium L (Solanaceae). Evolution 54:778–788CrossRefGoogle Scholar
  64. Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE, Parchman TL, Johnston JS et al (2014) Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344:738–742CrossRefGoogle Scholar
  65. Tabashnik BE, Carrière Y (2017) Surge in insect resistance to transgenic crops and prospects for sustainability. Nat Biotechnol 35:926–935CrossRefGoogle Scholar
  66. Valverde PL, Fornoni J, Núñez-Farfán J (2001) Defensive role of leaf trichomes in resistance to herbivorous insects in Datura stramonium. J Evol Biol 14:424–432CrossRefGoogle Scholar
  67. Wasserman SS, Futuyma DJ (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil. Evolution 35:605–617CrossRefGoogle Scholar
  68. Wink M (2000) Interference of alkaloids with neuroreceptors and ion channels. Stud Nat Prod Chem 21:3–122CrossRefGoogle Scholar
  69. Wink M, Schmeller T, Latz-Brüning B (1998) Modes of action of allelochemical alkaloids: interaction with neuroreceptors DNA and other molecular targets. J Chem Ecol 24:1881–1937CrossRefGoogle Scholar
  70. Winkler IS, Mitter C, Scheffer SJ (2009) Repeated climate-linked host shifts have promoted diversification in a temperate clade of leaf-mining flies. Proc Natl Acad Sci USA 106:18103–18108CrossRefGoogle Scholar
  71. Zangerl AR, Berenbaum MR (2005) Increase in toxicity of an invasive weed after reassociation with its coevolved herbivore. Proc Natl Acad Sci USA 102:15529–15532CrossRefGoogle Scholar
  72. Zhu F, Moural TW, Nelson DR, Palli SR (2016) A specialist herbivore pest adaptation to xenobiotics through up-regulation of multiple Cytochrome P450s. Sci Rep 6:20421CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoCoyoacán, Mexico CityMexico
  2. 2.Laboratory of Evolutionary Entomology, Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland
  3. 3.CONACYT. Red de EcoetologíaInstituto de Ecología A. C.XalapaMexico

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