Facultative endosymbionts of aphid populations from coastal dunes of the North Sea

Authors

  • Eduardo de la Peña Ghent University, Department of Biology, Terrestrial Ecology Unit, K.L. Ledeganckstraat 35, 9000 Gent
  • Viki Vandomme Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000 Brussels
  • Enric Frago Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen

DOI:

https://doi.org/10.26496/bjz.2014.64

Keywords:

wasps, parasitoids, heat shock, specific primers, top-down, bottom-up control

Abstract

Aphids establish symbiotic associations with a diverse assemblage of mutualistic bacteria. Some of them are not required for the host’s survival but still have a crucial impact on the biology and ecology of their host. Facultative symbionts may modify important host-life-history traits and affect the interactions of aphids with other members of the community. So far several species of aphid have been reported to occur in coastal dunes. Given the extreme environmental conditions of this type of habitat and the wide distribution along the European coast of some aphid species, these aphids would be expected to show variation in their facultative endosymbionts. However, there is currently no information available for these species. To address this question, we collected specimens from different populations of aphids (i.e. Schizaphis rufula, Laingia psammae and Rhopalosiphum padi) associated with the dune grass Ammophila arenaria in several locations of the North and the Irish Sea. By means of specific diagnostic PCR’s we checked for the presence of facultative bacterial endosymbionts in these populations. Results of this explorative assessment showed variation in the endosymbiont community according to species and location. All populations sampled along the North Sea coast were associated with the facultative endosymbiont Serratia symbiotica. Hamiltonella defensa was only detected in some specimens coming from the population in Het Zwin, Belgium. Regiella insecticola and the γ-protobacteria X-type were only found associated with the population of Schizaphis rufula in De Panne, Belgium. Although further experiments are necessary to characterize the nature of these symbiotic relationships, our correlation analyses showed a significant co-occurrence of S. symbiotica with H. defensa and R. insecticola with X-type protobacteria suggesting reciprocal regulatory functions. No significant correlation was detected between the number of mummies (i.e. carcasses of aphids parasitized by wasps) and the occurrence of bacterial symbionts. The potential role of these symbionts in coastal dune ecosystems is discussed.

References

Benson Da, Cavanaugh M, clark K, Karsch-Mizrachi I, lipman DJ, ostell J, sayers EW. (2013) GenBank. Nucleic Acids Research Jan; (D1) D36-42.

Bröring U. & Niedringhaus (1989) Die epigäische Hemipterenfauna (Heteroptera, Auchenorrhyncha) der Tertiärdünen Ostfriesischer Düneninseln. - Braunschw. naturk. Schr. 3: 387-398.

Brumin M, Kontsedalov S, Ghamin M. (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Science 18, 57-66.

Burke G, Hiehn O, Moran N (2010) Effects of facultative symbionts and heat stress on the metabolome of pea aphids. The ISME Journal 4:242-252.

de la Peña E, Karssen G, Moens M (2007) Diversity and distribution of root lesion nematodes associated to Ammophila arenaria in Europe dunes. Nematology, 9: 881-901.

de la Peña E, Bonte D, Moens M (2009) Evidence of population differentiation in the dune grass Ammophila arenaria and its associated root-feeding nematodes. Plant and Soil 324 (1-2): 307-316.

de la Peña E, Rodríguez-Echeverría S, Van der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by arbuscular mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytologist, 169:829-840.

Degnan PH, Yu Y, Sisneros N, Wing RA, Moran NA (2009) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proceedings of the National Academy of Sciences 106 (22): 9063–9068.

Ferrari J, Darby AC, Daniell TJ, Godfray HCJ, Douglas AE (2004) Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecological Entomology 29: 60-65.

Ferrari J, West JA, Godfray HCJ (2011) Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66(2): 375-390.

Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect-plant interactions. Trends in Ecology & Evolution, 27(12): 705-711.

Guay JF, Boudreault S, Michaud D, cloutier C (2009) Impact of environmental stress on aphid clonal resistance to parasitoids: Role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. Journal of Insect Physiology 55: 919-926.

Henry LM, Peccoud J, Simon JC, Hadfield JD, Maiden MJC, Ferrari J, Godfray HCJ (2013). Horizontally transmitted symbionts and host colonization of ecological niches. Current biology 23(17), 1713–7.

Jaber LR, Vidal S (2009) Interactions between and endophytic fungus, aphids and extrafloral nectaries: do endophytes induce extrafloral-mediated defenses in Vicia faba. Functional Ecology 23(4), 707-714.

Leonardo T E & Mondor EB (2006). Symbiont modifies host life history traits that affect gene flow. Proceedings of the Royal Society of London B – Biological Sciences 273: 1079-1084.

Lukasik P, Dawid MA, Ferrari J, Godfray hcj (2013) The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia 173: 985-996.

Maun M (2009) The biology of coastal sand dunes. Oxford University press.

McClean AHC, Van Asch M, Ferrari J, Godfray HCJ (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proc. R. Soc. B, 278: 760-766.

Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics. 42:165-90.

Nyabuga FN, Outreman Y, Simon J, Heckel DG, Weisser W (2010) Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomologia Experimentalis et Applicata 136: 243-253.

Oliver KM, Degnan PH, Burke GR, Moran NA (2010) Facultative symbionts in aphids and the horizontal transfer of ecological important traits. Annu. Rev. Entomol. 55:247-266.

Pettersson J (1971) Studies on four grass-inhabiting species of Schizaphis (Hem: Aphidoidea) II. Morphological descriptions of populations of S. dubia Huc., S. arrenatheri n. sp., S. rufula (Walk.) and S. longicaudata H.R.L. Swedish Journal of Agricultural Research I: 115-132.

Sakurai M, Koga R, Tsuchida T, Meng X, Fukatsu T (2005) Rickettsia s symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness and interaction with the essential symbiont Buchnera. Applied Environmental Microbiology 7: 4069-4075.

Scarborough CL, Ferrari J, Godfray HCJ (2005) Aphid protected from pathogen by endosymbiont. Science 310: 1781-1781.

Vandegehuchte M, De la Peña E, Bonte D (2010) Aphids on Ammophila arenaria in Belgium: firs t reports, phenology and host range expansion. Belgian Journal of Zoology, 140: 77-79.

Vandegehuchte M, De la Peña E, Bonte D (2010) Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field. Oikos, 119: 1011-10.

Vandegehuchte M, De la Peña E, Bonte D (2013). Non-local genotypes of a resident grass species reduce invertebrate species richness. Insect Conservation and Diversity 5(6): 453-460.

Vorburger C, Sandrock C, Gouskov A, Castañeda L, Ferrari J (2009) Genotypic variation and the role of defensive endosymbionts in an all-parthenogenetic host-parasitoid interaction. Evolution 63: 1439–50.

vorburger C, Gehrer L, Rodriguez P (2010) A strain of the bacterial symbiont Regiella insecticola protect against insect parasitoids. Biology letters 6: 109-112.

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Published

2020-01-13

How to Cite

de la Peña, E., Vandomme, V., & Frago, E. (2020). Facultative endosymbionts of aphid populations from coastal dunes of the North Sea. Belgian Journal of Zoology, 144(1). https://doi.org/10.26496/bjz.2014.64

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