Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Katharine F. Preedy
  • Mark A.J. Chaplain
  • Daniel J. Leybourne
  • Glenn Marion
  • Alison J. Karley

External Research Organisations

  • Biomathematics and Statistics Scotland
  • University of St. Andrews
  • The James Hutton Institute
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Details

Original languageEnglish
Pages (from-to)1216-1229
Number of pages14
JournalJournal of Animal Ecology
Volume89
Issue number5
Early online date25 Feb 2020
Publication statusPublished - 4 May 2020
Externally publishedYes

Abstract

Aphid populations frequently include phenotypes that are resistant to parasitism by hymenopterous parasitoid wasps, which is often attributed to the presence of ‘protective’ facultative endosymbionts residing in aphid tissues, particularly Hamiltonella defensa. In field conditions, under parasitoid pressure, the observed coexistence of aphids with and without protective symbionts cannot be explained by their difference in fitness alone. Using the cereal aphid Rhopalosiphum padi as a model, we propose an alternative mechanism whereby parasitoids are more efficient at finding common phenotypes of aphid and experience a fitness cost when switching to the less common phenotype. We construct a model based on delay differential equations and parameterize and validate the model with values within the ranges obtained from experimental studies. We then use it to explore the possible effects on system dynamics under conditions of environmental stress, using our existing data on the effects of drought stress in crops as an example. We show the ‘switching penalty’ incurred by parasitoids leads to stable coexistence of aphids with and without H. defensa and provides a potential mechanism for maintaining phenotypic diversity among host organisms. We show that drought-induced reduction in aphid development time has little impact. However, greater reduction in fecundity on droughted plants of symbiont-protected aphids can cause insect population cycles when the system would be stable in the absence of drought stress. The stabilizing effect of the increased efficiency in dealing with more commonly encountered host phenotypes is applicable to a broad range of consumer–resource systems and could explain stable coexistence in competitive environments. The loss of stable coexistence when drought has different effects on the competing aphid phenotypes highlights the importance of scenario testing when considering biocontrol for pest management.

Keywords

    climate change, drought, Hamiltonella defensa, mathematical model, parasitoid, symbiont

ASJC Scopus subject areas

Sustainable Development Goals

Cite this

Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress. / Preedy, Katharine F.; Chaplain, Mark A.J.; Leybourne, Daniel J. et al.
In: Journal of Animal Ecology, Vol. 89, No. 5, 04.05.2020, p. 1216-1229.

Research output: Contribution to journalArticleResearchpeer review

Preedy KF, Chaplain MAJ, Leybourne DJ, Marion G, Karley AJ. Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress. Journal of Animal Ecology. 2020 May 4;89(5):1216-1229. Epub 2020 Feb 25. doi: 10.1111/1365-2656.13189
Preedy, Katharine F. ; Chaplain, Mark A.J. ; Leybourne, Daniel J. et al. / Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress. In: Journal of Animal Ecology. 2020 ; Vol. 89, No. 5. pp. 1216-1229.
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title = "Learning-induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress",
abstract = "Aphid populations frequently include phenotypes that are resistant to parasitism by hymenopterous parasitoid wasps, which is often attributed to the presence of {\textquoteleft}protective{\textquoteright} facultative endosymbionts residing in aphid tissues, particularly Hamiltonella defensa. In field conditions, under parasitoid pressure, the observed coexistence of aphids with and without protective symbionts cannot be explained by their difference in fitness alone. Using the cereal aphid Rhopalosiphum padi as a model, we propose an alternative mechanism whereby parasitoids are more efficient at finding common phenotypes of aphid and experience a fitness cost when switching to the less common phenotype. We construct a model based on delay differential equations and parameterize and validate the model with values within the ranges obtained from experimental studies. We then use it to explore the possible effects on system dynamics under conditions of environmental stress, using our existing data on the effects of drought stress in crops as an example. We show the {\textquoteleft}switching penalty{\textquoteright} incurred by parasitoids leads to stable coexistence of aphids with and without H. defensa and provides a potential mechanism for maintaining phenotypic diversity among host organisms. We show that drought-induced reduction in aphid development time has little impact. However, greater reduction in fecundity on droughted plants of symbiont-protected aphids can cause insect population cycles when the system would be stable in the absence of drought stress. The stabilizing effect of the increased efficiency in dealing with more commonly encountered host phenotypes is applicable to a broad range of consumer–resource systems and could explain stable coexistence in competitive environments. The loss of stable coexistence when drought has different effects on the competing aphid phenotypes highlights the importance of scenario testing when considering biocontrol for pest management.",
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AU - Preedy, Katharine F.

AU - Chaplain, Mark A.J.

AU - Leybourne, Daniel J.

AU - Marion, Glenn

AU - Karley, Alison J.

N1 - Funding Information: The authors gratefully acknowledge financial support by the Scottish Government through the Strategic Research Programme of the Scottish Government's Rural and Environment Science and Analytical Services Division (RESAS). D.J.L. was funded by the James Hutton Institute and the Universities of Aberdeen and Dundee through a Scottish Food Security Alliance (Crops) PhD studentship.

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