A fitness cost resulting from Hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi

Daniel J. Leybourne, Tracy A. Valentine, Jorunn I. B. Bos, Alison J. Karley (Lead / Corresponding author)

Research output: Contribution to journalArticle

Abstract

Many herbivorous arthropods, including aphids, frequently associate with facultative endosymbiotic bacteria, which influence arthropod physiology and fitness. In aphids, endosymbionts can increase resistance against natural enemies, enhance aphid virulence and alter aphid fitness. Here, we used the electrical penetration graph technique to uncover physiological processes at the insect-plant interface affected by endosymbiont infection. We monitored the feeding and probing behaviour of four independent clonal lines of the cereal-feeding aphid Rhopalosiphum padi derived from the same multilocus genotype containing differential infection (+/-) with a common facultative endosymbiont, Hamiltonella defensa Aphid feeding was examined on a partially resistant wild relative of barley known to impair aphid fitness and a susceptible commercial barley cultivar. Compared with uninfected aphids, endosymbiont-infected aphids on both plant species exhibited a twofold increase in the number of plant cell punctures, a 50% reduction in the duration of each cellular puncture and a twofold higher probability of achieving sustained phloem ingestion. Feeding behaviour was also altered by host plant identity: endosymbiont-infected aphids spent less time probing plant tissue, required twice as many probes to reach the phloem and showed a 44% reduction in phloem ingestion when feeding on the wild barley relative compared with the susceptible commercial cultivar. Reduced feeding success could explain the 22% reduction in growth of H. defensa-infected aphids measured on the wild barley relative. This study provides the first demonstration of mechanisms at the aphid-plant interface contributing to physiological effects of endosymbiont infection on aphid fitness, through altered feeding processes on different quality host plants.

Original languageEnglish
Article number207936
Pages (from-to)1-11
Number of pages11
JournalJournal of Experimental Biology
Volume223
Issue number1
Early online date10 Dec 2019
DOIs
Publication statusPublished - 2 Jan 2020

Fingerprint

Rhopalosiphum padi
Aphids
Feeding Behavior
feeding behavior
aphid
Aphidoidea
fitness
Costs and Cost Analysis
endosymbiont
Infection
endosymbionts
cost
infection
Hordeum
Phloem
barley
phloem
Arthropods
Punctures
arthropod

Keywords

  • Electrical penetration graph
  • EPG
  • Facultative
  • endosymbiont
  • Insect physiology
  • Symbiosis

Cite this

@article{285dae47e9d94f1ca1b35702edcfa4c3,
title = "A fitness cost resulting from Hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi",
abstract = "Many herbivorous arthropods, including aphids, frequently associate with facultative endosymbiotic bacteria, which influence arthropod physiology and fitness. In aphids, endosymbionts can increase resistance against natural enemies, enhance aphid virulence and alter aphid fitness. Here, we used the electrical penetration graph technique to uncover physiological processes at the insect-plant interface affected by endosymbiont infection. We monitored the feeding and probing behaviour of four independent clonal lines of the cereal-feeding aphid Rhopalosiphum padi derived from the same multilocus genotype containing differential infection (+/-) with a common facultative endosymbiont, Hamiltonella defensa Aphid feeding was examined on a partially resistant wild relative of barley known to impair aphid fitness and a susceptible commercial barley cultivar. Compared with uninfected aphids, endosymbiont-infected aphids on both plant species exhibited a twofold increase in the number of plant cell punctures, a 50{\%} reduction in the duration of each cellular puncture and a twofold higher probability of achieving sustained phloem ingestion. Feeding behaviour was also altered by host plant identity: endosymbiont-infected aphids spent less time probing plant tissue, required twice as many probes to reach the phloem and showed a 44{\%} reduction in phloem ingestion when feeding on the wild barley relative compared with the susceptible commercial cultivar. Reduced feeding success could explain the 22{\%} reduction in growth of H. defensa-infected aphids measured on the wild barley relative. This study provides the first demonstration of mechanisms at the aphid-plant interface contributing to physiological effects of endosymbiont infection on aphid fitness, through altered feeding processes on different quality host plants.",
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note = "DJL was funded by the James Hutton Institute and the Universityies of Aberdeen and Dundee through a Scottish Food Security Alliance (Crops) PhD studentship. AJK and TAV were supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division. JIBB was supported by the European Research Council (310190-APHIDHOST).",
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A fitness cost resulting from Hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi. / Leybourne, Daniel J.; Valentine, Tracy A.; Bos, Jorunn I. B.; Karley, Alison J. (Lead / Corresponding author).

In: Journal of Experimental Biology, Vol. 223, No. 1, 207936, 02.01.2020, p. 1-11.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A fitness cost resulting from Hamiltonella defensa infection is associated with altered probing and feeding behaviour in Rhopalosiphum padi

AU - Leybourne, Daniel J.

AU - Valentine, Tracy A.

AU - Bos, Jorunn I. B.

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