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.

AU - Karley, Alison J.

N1 - Funding Information: D.J.L. was funded by the James Hutton Institute and the University of Aberdeen and University of Dundee and Dundee through a Scottish Food Security Alliance (Crops) PhD studentship. A.J.K. and T.A.V. were supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division. J.I.B.B. was supported by the European Research Council (310190-APHIDHOST).

PY - 2020

Y1 - 2020

N2 - 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.

AB - 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.

KW - Electrical penetration graph

KW - EPG

KW - Facultative endosymbiont

KW - Insect physiology

KW - Symbiosis

UR - http://www.scopus.com/inward/record.url?scp=85077477939&partnerID=8YFLogxK

U2 - 10.1242/jeb.207936

DO - 10.1242/jeb.207936

M3 - Article

C2 - 31822555

AN - SCOPUS:85077477939

VL - 223

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 1

M1 - jeb207936

ER -