TY - JOUR

T1 - The price of protection

T2 - a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid, Rhopalosiphum padi

AU - Leybourne, Daniel J.

AU - Bos, Jorunn I.B.

AU - Valentine, Tracy A.

AU - Karley, Alison J.

N1 - Funding Information: DJL was funded by the James Hutton Institute and the Universities of Aberdeen and Dundee through a Scottish Food Security Alliance (Crops) PhD studentship. AJK and TAV were funded through the strategic research programme funded by the Scottish Government's Rural and Environment Science and Analytical Services Division. JIBB was funded through a Royal Society of Edinburgh Personal Fellowship and an ERC starting grant (APHIDHOST). We thank Gaynor Malloch (James Hutton Institute) and Brian Fenton (Scotland's Rural College) for supplying aphid line “JB,” with additional thanks to Gaynor Malloch for advice on microsatellite scoring. We also thank Stephen Hubbard (University of Dundee) for statistical advice, Rob Hancock (James Hutton Institute) for helpful comments on the manuscript, and three anonymous reviewers for their comments and advice to improve the manuscript.

PY - 2019/9/17

Y1 - 2019/9/17

N2 - Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont-infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.

AB - Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L-type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa-infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont-infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.

KW - cereal aphid

KW - Hamiltonella defensa

KW - Hordeum spontaneum

KW - Hordeum vulgare

KW - symbiosis

UR - http://www.scopus.com/inward/record.url?scp=85072509450&partnerID=8YFLogxK

U2 - 10.1111/1744-7917.12606

DO - 10.1111/1744-7917.12606

M3 - Article

C2 - 29797656

AN - SCOPUS:85072509450

VL - 27

SP - 69

EP - 85

JO - Insect Science

JF - Insect Science

SN - 1672-9609

IS - 1

ER -