Grain aphid clones vary in frost resistance, but this trait is not influenced by facultative endosymbionts

Ecological Entomology

Volumn 36, Issue 6, 2011, Pages 790-793

  Lukasik, Piotr ^a   Hancock, Emily L ^a   Ferrari, Julia ^a,b   Godfray, H Charles J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Acyrthosiphon pisum pea aphid; Cold hardiness; Hamiltonella defensa; Regiella insecticola; Secondary endosymbionts; Sitobion avenae grain aphid

Indexed keywords

APHID; BACTERIUM; CLONE; CROP PEST; ENDOSYMBIONT; FACULTATIVE BEHAVIOR; FITNESS; FROST HARDINESS; GENOTYPE-ENVIRONMENT INTERACTION; HERITABILITY; HOST-SYMBIONT INTERACTION; LIFE HISTORY TRAIT; LOW TEMPERATURE; PHYSIOLOGY; SURVIVAL;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS); CANDIDATUS HAMILTONELLA DEFENSA; CANDIDATUS REGIELLA INSECTICOLA; HEXAPODA; PISUM SATIVUM; SITOBION AVENAE;

EID: 81855166953     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2011.01321.x     Document Type: Article

References (32)

1. Bale, J.S. (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 357, 849-861.
2. Bensadia, F., Boudreault, S., Guay, J.-F., Michaud, D. & Cloutier, C. (2006) Aphid clonal resistance to a parasitoid fails under heat stress. Journal of Insect Physiology, 52, 146-157.
3. Burke, G., Fiehn, O. & Moran, N. (2010) Effects of facultative symbionts and heat stress on the metabolome of pea aphids. Isme Journal, 4, 242-252.
4. Dedryver, C.A., Hulle, M., Le Gallic, J.F., Caillaud, M.C. & Simon, J.C. (2001) Coexistence in space and time of sexual and asexual populations of the cereal aphid Sitobion avenae. Oecologia, 128, 379-388.
5. Dewar, A.M. & Carter, N. (1984) Decision trees to assess the risk of cereal aphid (Hemiptera: Aphididae) outbreaks in summer in England. Bulletin of Entomological Research, 74, 387-398.
6. Doucet, D., Walker, V.K. & Qin, W. (2009) The bugs that came in from the cold: molecular adaptations to low temperatures in insects. Cellular and Molecular Life Sciences, 66, 1404-1418.
7. Dunbar, H.E., Wilson, A.C.C., Ferguson, N.R. & Moran, N.A. (2007) Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol, 5, e96.
8. Griffiths, E. & Wratten, S.D. (1979) Intra- and inter-specific differences in cereal aphid low-temperature tolerance. Entomologia Experimentalis et Applicata, 26, 161-167.
9. Guay, J.F., 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.
10. Knight, J.D. & Bale, J.S. (1986) Cold hardiness and overwintering of the grain aphid Sitobion avenae. Ecological Entomology, 11, 189-197.
11. Lee, R.E., Stronggunderson, J.M., Lee, M.R. & Davidson, E.C. (1992) Ice-nucleating active bacteria decrease the cold hardiness of stored grain insects. Journal of Economic Entomology, 85, 371-374.
12. Lee, R.E., Lee, M.R. & Stronggunderson, J.M. (1993) Insect cold-hardiness and ice nucleating active microorganisms, including their potential use for biological control. Journal of Insect Physiology, 39, 1-12.
13. Leonardo, T.E. (2004) Removal of a specialization-associated symbiont does not affect aphid fitness. Ecology Letters, 7, 461-468.
14. Leonardo, T.E. & Mondor, E.B. (2006) Symbiont modifies host life-history traits that affect gene flow. Proceedings of the Royal Society B: Biological Sciences, 273, 1079-1084.
15. Llewellyn, K.S., Loxdale, H.D., Harrington, R., Brookes, C.P., Clark, S.J. & Sunnucks, P. (2003) Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites. Molecular Ecology, 12, 21-34.
16. McLean, A.H.C., van Asch, M., Ferrari, J. & Godfray, H.C.J. (2011) Effects of bacterial secondary symbionts on host plant use in pea aphids. Proceedings of the Royal Society B: Biological Sciences, 278, 760-766.
17. Montllor, C.B., Maxmen, A. & Purcell, A.H. (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecological Entomology, 27, 189-195.
18. Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190.
19. Neelakanta, G., Sultana, H., Fish, D., Anderson, J.F. & Fikrig, E. (2010) Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. Journal of Clinical Investigation, 120, 3179-3190.
20. Newton, C. & Dixon, A.F.G. (1988) A preliminary study of variation and inheritance of life history traits and the occurence of hybrid vigor in Sitobion avenae (F.) (Hemiptera, Aphididae). Bulletin of Entomological Research, 78, 75-83.
21. Ohtaka, C. & Ishikawa, H. (1991) Effects of heat treatment on the symbiotic system of an aphid mycetocyte. Symbiosis, 11, 19-30.
22. Oliver, K.M., Degnan, P.H., Burke, G.R. & Moran, N.A. (2010) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annual Review of Entomology, 55, 247-66.
23. Papura, D., Simon, J.C., Halkett, F., Delmotte, F., Le Gallic, J.F. & Dedryver, C.A. (2003) Predominance of sexual reproduction in Romanian populations of the aphid Sitobion avenae inferred from phenotypic and genetic structure. Heredity, 90, 397-404.
24. Parish, W.E.G. & Bale, J.S. (1991) Effect of low temperatures on the intracellular symbionts of the grain aphid Sitobion avenae (F.) (Hem., Aphididae). Journal of Insect Physiology, 37, 339-345.
25. Parish, W.E.G. & Bale, J.S. (1993) Effects of brief exposures to low temperature on the development, longevity and fecundity of the grain aphid Sitobion avenae (Hemiptera, Aphididae). Annals of Applied Biology, 122, 9-21.
26. Powell, S.J. & Bale, J.S. (2004) Cold shock injury and ecological costs of rapid cold hardening in the grain aphid Sitobion avenae (Hemiptera: Aphididae). Journal of Insect Physiology, 50, 277-284.
27. R Development Core Team (2011) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL.
28. Radcliffe Meteorological Station (2011) Radcliffe Weather Station annual reports [WWW document]. URL [accessed on 18 July 2011].
29. Russell, J.A. & Moran, N.A. (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proceedings of the Royal Society B: Biological Sciences, 273, 603-610.
30. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. & Fukatsu, T. (2002) Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Molecular Ecology, 11, 2123-2135.
31. Tsuchida, T., Koga, R., Horikawa, M., Tsunoda, T., Maoka, T., Matsumoto, S. et al. (2010) Symbiotic bacterium modifies aphid body color. Science, 330, 1102-1104.
32. Vorburger, C. (2004) Cold tolerance in obligate and cyclical parthenogens of the peach-potato aphid, Myzus persicae. Ecological Entomology, 29, 498-505.