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An aphid symbiont confers protection against a specialized RNA virus, another increases vulnerability to the same pathogen
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  • Clesson Higashi,
  • William Nichols,
  • Germain Chevignon,
  • Vilas Patel,
  • Kyungsun Kim,
  • Suzanne Allison ,
  • Michael Strand,
  • Kerry Oliver
Clesson Higashi
University of Georgia Department of Entomology

Corresponding Author:[email protected]

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William Nichols
University of Georgia
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Germain Chevignon
Ifremer Laboratoire de Génétique et Pathologie des Mollusques Marins
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Vilas Patel
University of Georgia
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Kyungsun Kim
University of Georgia
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Suzanne Allison
University of Georgia Department of Entomology
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Michael Strand
University of Georgia
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Kerry Oliver
University of Georgia Department of Entomology
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Insects often harbor heritable symbionts that provide defense against specialized natural enemies, yet little is known about symbiont protection when hosts face simultaneous threats. In pea aphids (Acyrthosiphon pisum), the facultative endosymbiont Hamiltonella defensa confers protection against the parasitoid, Aphidius ervi, and Regiella insecticola protects against aphid-specific fungal pathogens, including Pandora neoaphidis. Here we investigated whether these two common aphid symbionts protect against a specialized virus A. pisum virus (APV), and whether their anti-fungal and anti-parasitoid services are impacted by APV infection. We found that APV imposed large fitness costs on symbiont-free aphids and these costs were elevated in aphids housing H. defensa. In contrast, APV titers were significantly reduced and costs to APV infection were largely eliminated in aphids with R. insecticola. To our knowledge, R. insecticola is the first aphid symbiont shown to protect against a viral pathogen, and only the second arthropod symbiont reported to do so. In contrast, APV infection did not impact the protective services either R. insecticola or H. defensa. To better understand APV biology, we produced five genomes and examined transmission routes. We found that moderate rates of vertical transmission, combined with horizontal transfer through food plants, were the major route of APV spread, although lateral transfer by parasitoids also occurred. Transmission was unaffected by facultative symbionts. In summary, the presence and species identity of facultative symbionts resulted in highly divergent outcomes for aphids infected with APV, while not impacting defensive services that target other enemies. These findings add to the diverse phenotypes conferred by aphid symbionts, and to the growing body of work highlighting extensive variation in symbiont-mediated interactions.
29 Jun 2022Submitted to Molecular Ecology
01 Jul 2022Submission Checks Completed
01 Jul 2022Assigned to Editor
14 Jul 2022Reviewer(s) Assigned
09 Aug 2022Review(s) Completed, Editorial Evaluation Pending
31 Aug 2022Editorial Decision: Revise Minor
30 Oct 2022Review(s) Completed, Editorial Evaluation Pending
30 Oct 20221st Revision Received
30 Oct 2022Reviewer(s) Assigned
21 Nov 2022Editorial Decision: Revise Minor
24 Nov 2022Review(s) Completed, Editorial Evaluation Pending
24 Nov 20222nd Revision Received
29 Nov 2022Editorial Decision: Accept