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Where you come from matters: temperature influences host–parasitoid interaction through parental effects


Temperature alters host suitability for parasitoid development through direct and indirect pathways. Direct effects depend on ambient temperatures experienced by a single host individual during its lifetime. Indirect effects (or parental effects) occur when thermal conditions met by a host parental generation affect the way its offspring will interact with parasitoids. Using the complex involving eggs of the moth Lobesia botrana as hosts for the parasitoid Trichogramma cacoeciae, we developed an experimental design to disentangle the effects of (1) host parental temperature (temperature at which the host parental generation developed and laid host eggs) and (2) host offspring temperature (temperature at which host eggs were incubated following parasitism, i.e. direct thermal effects) on this interaction. The host parental generation was impacted by temperature experienced during its development: L. botrana females exposed to warmer conditions displayed a lower pupal mass but laid more host eggs over a 12-h period. Host parental temperature also affected the outcomes of the interaction. Trichogramma cacoeciae exhibited lower emergence rates but higher hind tibia length on emergence from eggs laid under warm conditions, even if they were themselves exposed to cooler temperatures. Such indirect thermal effects might arise from a low nutritional quality and/or a high immunity of host eggs laid in warm conditions. By contrast with host parental temperature, offspring temperature (direct thermal effects) did not significantly affect the outcomes of the interaction. This work emphasises the importance of accounting for parental thermal effects to predict the future of trophic dynamics under global warming scenarios.

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  1. Abdel-latief M, Hilker M (2008) Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect Biochem Mol Biol 38:136–145.

  2. Bahar MH, Soroka JJ, Dosdall LM (2012) Constant versus fluctuating temperatures in the interactions between Plutella xylostella (Lepidoptera: Plutellidae) and its larval parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Environ Entomol 41:1653–1661.

  3. Barnay O, Hommay G, Gertz C, Kienlen JC, Schubert G, Marro JP, Pizzol J, Chavigny P (2001) Survey of natural populations of Trichogramma (Hym., Trichogrammatidae) in the vineyards of Alsace (France). J Appl Entomol 125:469–477.

  4. Beaumont LJ, Hughes L, Pitman AJ (2008) Why is the choice of future climate scenarios for species distribution modelling important? Ecol Lett 11:1135–1146.

  5. Delava E, Fleury F, Gibert P (2016) Effects of daily fluctuating temperatures on the DrosophilaLeptopilina boulardi parasitoid association. J Therm Biol 60:95–102.

  6. Donelson JM, Salinas S, Munday PL, Shama LNS (2018) Transgenerational plasticity and climate change experiments: where do we go from here? Glob Change Biol 24:13–34.

  7. Doyon J, Boivin G (2005) The effect of development time on the fitness of female Trichogramma evanescens. J Insect Sci 5:4–9.

  8. Eggert H, Diddens-de Buhr MF, Kurtz J (2015) A temperature shock can lead to trans-generational immune priming in the red flour beetle, Tribolium castaneum. Ecol Evol 5:1318–1326.

  9. Fournier F, Boivin G (2000) Comparative dispersal of Trichogramma evanescens and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in relation to environmental conditions. Environ Entomol 29:55–63.

  10. Furlong MJ, Zalucki MP (2017) Climate change and biological control: the consequences of increasing temperatures on host–parasitoid interactions. Curr Opin Insect Sci 20:39–44.

  11. Geister TL, Lorenz MW, Hoffmann KH, Fischer K (2009) Energetics of embryonic development: effects of temperature on egg and hatchling composition in a butterfly. J Comp Physiol B 179:87–98.

  12. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton

  13. Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126.

  14. Harris RMB, Grose MR, Lee G, Bindoff NL, Porfirio LL, Fox-Hughes P (2014) Climate projections for ecologists. Wires Clim Change 5:621–637.

  15. Howe RW (1967) Temperature effects on embryonic development in insects. Annu Rev Entomol 12:15–42.

  16. Hutchison WD, Moratorio M, Martin JM (1990) Morphology and biology of Trichogrammatoidea bactrae (Hymenoptera: Trichogrammatidae), imported from Australia as a parasitoid of pink bollworm (Lepidoptera: Gelechiidae) eggs. Ann Entomol Soc Am 83:46–54.

  17. Iltis C, Martel G, Thiéry D, Moreau J, Louâpre P (2018) When warmer means weaker: high temperatures reduce behavioural and immune defences of the larvae of a major grapevine pest. J Pest Sci 91:1315–1326.

  18. Iltis C, Louâpre P, Pecharová K, Thiéry D, Zito S, Bois B, Moreau J (2019) Are life-history traits equally affected by global warming? A case study combining a multi-trait approach with fine-grain climate modeling. J Insect Physiol 117:103916.

  19. Janowitz SA, Fischer K (2011) Opposing effects of heat stress on male versus female reproductive success in Bicyclus anynana butterflies. J Therm Biol 36:283–287.

  20. Jeffs CT, Lewis OT (2013) Effects of climate warming on host–parasitoid interactions. Ecol Entomol 38:209–218.

  21. Kishani Farahani H, Ashouri A, Zibaee A, Abroon P, Alford L (2016) The effect of host nutritional quality on multiple components of Trichogramma brassicae fitness. Bull Entomol Res 106:633–641.

  22. Moreau J, Benrey B, Thiéry D (2006) Grape variety affects larval performance and also female reproductive performance of the European grapevine moth Lobesia botrana (Lepidoptera: Tortricidae). Bull Entomol Res 96:205–212.

  23. Moreau J, Richard A, Benrey B, Thiéry D (2009) Host plant cultivar of the grapevine moth Lobesia botrana affects the life history traits of an egg parasitoid. Biol Control 50:117–122.

  24. Moreau J, Monceau K, Thiéry D (2016) Larval food influences temporal oviposition and egg quality traits in females of Lobesia botrana. J Pest Sci 89:439–448.

  25. Moreno F, Pérez-Moreno I, Marco V (2009) Effects of Lobesia botrana (Lepidoptera: Tortricidae) egg age, density, and UV treatment on parasitism and development of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). Environ Entomol 38:1513–1520.

  26. Muller K, Arenas L, Thiéry D, Moreau J (2016) Direct benefits from choosing a virgin male in the European grapevine moth, Lobesia botrana. Anim Behav 114:165–172.

  27. Nardi JB (2004) Embryonic origins of the two main classes of hemocytes—granular cells and plasmatocytes—in Manduca sexta. Dev Genes Evol 214:19–28.

  28. Olson DM, Andow DA (1998) Larval crowding and adult nutrition effects on longevity and fecundity of female Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). Environ Entomol 27:508–514.

  29. Pizzol J, Pintureau B (2008) Effect of photoperiod experienced by parents on diapause induction in Trichogramma cacoeciae. Entomol Exp Appl 127:72–77.

  30. Pizzol J, Khoualdia O, Ferran A, Chavigny P, Vanlerbeghe-Masutti F (2005) A single molecular marker to distinguish between strains of Trichogramma cacoeciae. Biocontrol Sci Technol 15:527–531.

  31. Pizzol J, Desneux N, Wajnberg E, Thiéry D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496.

  32. Pomfret JC, Knell RJ (2006) Immunity and the expression of a secondary sexual trait in a horned beetle. Behav Ecol 17:466–472.

  33. Schreven SJJ, Frago E, Stens A, de Jong PW, van Loon JPA (2017) Contrasting effects of heat pulses on different trophic levels, an experiment with a herbivore-parasitoid model system. PLoS One 12:e0176704.

  34. Seehausen LM, Cusson M, Régnière J, Bory M, Stewart D, Djoumad A, Smith SM, Martel V (2017) High temperature induces downregulation of polydnavirus gene transcription in lepidopteran host and enhances accumulation of host immunity gene transcripts. J Insect Physiol 98:126–133.

  35. Sgrò CM, Terblanche JS, Hoffmann AA (2016) What can plasticity contribute to insect responses to climate change? Annu Rev Entomol 61:433–451.

  36. Stireman JO, Dyer LA, Janzen DH, Singer MS, Lill JT, Marquis J, 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. Proc Natl Acad Sci USA 102:17384–17387.

  37. Strand MR, Pech LL (1995) Immunological basis for compatibility in parasitoid–host relationships. Annu Rev Entomol 40:31–56.

  38. Thiéry D, Desneux N (2018) Host plants of the polyphagous grape berry moth Lobesia botrana during larval stage modulate moth egg quality and subsequent parasitism by the parasitoid Trichogramma cacoeciae. Entomol Gen 38:47–59.

  39. Thiéry D, Moreau J (2005) Relative performance of European grapevine moth (Lobesia botrana) on grapes and other hosts. Oecologia 143:548–557.

  40. Thiéry D, Monceau K, Moreau J (2014) Larval intraspecific competition for food in the European grapevine moth Lobesia botrana. Bull Entomol Res 104:517–524.

  41. Thiéry D, Louâpre P, Muneret L, Rusch A, Sentenac G, Vogelweith F, Iltis C, Moreau J (2018) Biological protection against grape berry moths. A review. Agron Sustain Dev 38:15.

  42. Thomson LJ, Macfadyen S, Hoffmann AA (2010) Predicting the effects of climate change on natural enemies of agricultural pests. Biol Control 52:296–306.

  43. Trauer-Kizilelma U, Hilker M (2015) Impact of transgenerational immune priming on the defence of insect eggs against parasitism. Dev Comp Immunol 51:126–133.

  44. Triggs AM, Knell RJ (2012) Parental diet has strong transgenerational effects on offspring immunity. Funct Ecol 26:1409–1417.

  45. van Baaren J, Le Lann C, van Alphen J (2010) Consequences of climate change for aphid-based multi-trophic systems. In: Kindlmann P, Dixon AFG, Michaud JP (eds) Aphid biodiversity under environmental change. Springer, Dordrecht, pp 55–68.

  46. Vinson SB, Iwantsch GF (1980) Host suitability for insect parasitoids. Annu Rev Entomol 25:397–419.

  47. Visser B, Ellers J (2008) Lack of lipogenesis in parasitoids: a review of physiological mechanisms and evolutionary implications. J Insect Physiol 54:1315–1322.

  48. Vogelweith F, Thiéry D, Moret Y, Colin E, Motreuil S, Moreau J (2014) Defense strategies used by two sympatric vineyard moth pests. J Insect Physiol 64:54–61.

  49. Walker M, Jones TH (2001) Relative roles of top–down and bottom–up forces in terrestrial tritrophic plant-insect herbivore-natural enemy systems. Oikos 93:177–187.

  50. Woestmann L, Saastamoinen M (2016) The importance of trans-generational effects in Lepidoptera. Curr Zool 62:489–499.

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We are grateful to thank Géraldine Groussier for providing the parasitoid strains used in the experiments, Sébastien Zito and Benjamin Bois for providing the climatic data. We acknowledge the valuable contribution of Alexandre Bauer, Aude Balourdet, Hugo Baali, Léa Bariod and Martin Pêcheur during the experiments. We would also like to thank the handling editor George Heimpel and the two anonymous reviewers for their insightful comments and helpful suggestions on the manuscript. This work was supported by the Conseil Régional de Bourgogne Franche-Comté through the Plan d’Actions Régional pour l’Innovation (PARI) and two other funding sources (FABER LOUAPRE-AGREE-BGS and VALEACLIM-BOIS), and the European Union through the PO FEDER-FSE Bourgogne 2014/2020 programs.

Author information

All authors conceived and designed the experiments. CI and CM: performed the experiments; CI, CM and PL: analysed the data; CI, PL and JM: led the writing of the manuscript. All authors critically revised the intellectual content of the draft and gave their approbation for the final version to be published.

Correspondence to Corentin Iltis.

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The authors declare they have no conflict of interest.

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All applicable institutional and/or national guidelines for the care and use of animals were followed.

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Communicated by George Heimpel.

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Iltis, C., Moreau, J., Manière, C. et al. Where you come from matters: temperature influences host–parasitoid interaction through parental effects. Oecologia (2020).

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  • Host eggs
  • Oophagous parasitoid
  • Parental effects
  • Temperature
  • Trophic dynamics