Harbouring the secondary endosymbiont Regiella insecticola increases predation risk and reproduction in the cereal aphid Sitobion avenae

  • Guillermo E. Ramírez-Cáceres
  • Mario G. Moya-Hernández
  • Manuel Quilodrán
  • Roberto F. Nespolo
  • Ricardo Ceballos
  • Cristian A. Villagra
  • Claudio C. RamírezEmail author
Original Paper


Symbiosis in insects has been recognized as contributing to their ecological and evolutionary success. In the case of agricultural pests, endosymbionts may help insects colonize and expand their niches, allowing them to use different crops and to confront climatic variation. Moreover, endosymbionts provide improved defences against pathogens, predators, and parasitoids. In aphids, facultative endosymbionts have been found capable of generating these characteristics. However, evidence for this has been gathered from only a few model organisms. Here, we studied the effect of the facultative endosymbiont Regiella insecticola on the predation of Sitobion avenae clones by the ladybird Hippodamia variegata. In the laboratory, we assessed the predation rate of this coccinellid and the concomitant anti-predator behaviour of S. avenae with and without R. insecticola. We also evaluated the effect of the presence of this endosymbiont on the constitutive levels of E-β-farnesene, on the metabolic rate, and on the reproductive performance of S. avenae. All these traits were studied on two common alternative crops: wheat and barley. We found that R. insecticola-infected aphids were more predated irrespective of host plants and did not improve defences against coccinellid predators or metabolic rates on any host plants. Levels of E-β-farnesene were higher on wheat plants, irrespective of the presence of R. insecticola. Interestingly, R. insecticola-infected aphids had increased performance on wheat, while the opposite was true on barley. We discuss our findings based on the importance of secondary symbionts as providers of traits allowing aphids to be very invasive crop pests worldwide.


Symbiosis Metabolic rate Predator Multitrophic interactions 



We thank Francisca Zepeda-Paulo for allowing the use of the aphid clone she collected and maintained in the laboratory. This work was funded by FONDECYT grants 1131008 to CCR and Iniciativa Científica Milenio NC120027.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Ecología, Facultad de Ciencias BiológicasPontificia Universidad Católica de ChileSantiagoChile
  2. 2.Centro de Ecología Molecular y Funcional, Instituto de Ciencias BiológicasUniversidad de TalcaTalcaChile
  3. 3.Instituto de Ciencias Ambientales y EvolutivasUniversidad Austral de ChileValdiviaChile
  4. 4.Center of Applied Ecology and Sustainability (CAPES), Departamento de Ecología, Facultad de Ciencias BiológicasUniversidad Católica de ChileSantiagoChile
  5. 5.Millennium Institute for Integrative Biology (iBio)SantiagoChile
  6. 6.Laboratorio de Ecología Química, Instituto de Investigaciones AgropecuariasCRI-QuilamapuChillánChile
  7. 7.Instituto de EntomologíaUniversidad Metropolitana de Ciencias de la EducaciónSantiagoChile

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