Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-30T23:09:06.208Z Has data issue: false hasContentIssue false
  • English
  • Français

Evidence of plastic probing behavior in a ‘superclone’ of the grain aphid Sitobion avenae

Published online by Cambridge University Press:  30 August 2016

J. Barrios-SanMartín ,
C.C. Figueroa  and
C.C. Ramírez
J. Barrios-SanMartín
Affiliation:
Millennium Nucleus Center in Molecular Ecology and Evolutionary Applications in the Agroecosystems, Instituto de Ciencias Biológicas, Universidad de Talca, 2 Norte 685, Talca, Chile
C.C. Figueroa
Affiliation:
Millennium Nucleus Center in Molecular Ecology and Evolutionary Applications in the Agroecosystems, Instituto de Ciencias Biológicas, Universidad de Talca, 2 Norte 685, Talca, Chile
C.C. Ramírez*
Affiliation:
Millennium Nucleus Center in Molecular Ecology and Evolutionary Applications in the Agroecosystems, Instituto de Ciencias Biológicas, Universidad de Talca, 2 Norte 685, Talca, Chile
*
*Author for correspondence Telephone: 56-71-2200-289 Fax: 56-71-2200-276 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Asexual reproduction is very common in invasive insect pest. In the recent years, increasing evidences have shown that some invasive asexual lineages display an outstanding capacity to predominate in space and persist on time (superclones). However, little is known about the host-use behavior of these superclones. The English grain aphid Sitobion avenae (Fabricius) (Hemiptera: Aphididae) is one of the major pests of cereals worldwide. Chilean populations of the grain aphid are characterized by a high degree of heterozygosity and low genotypic variability across regions and years, with only four predominant superclone genotypes representing nearly 90% of populations. In this study, (1) the reproductive performance and (2) the probing behavior followed a host shift of one superclone and one non-superclone of S. avenae, were compared. The host plant in the superclone did not affect the reproductive performance, while in the non-superclone was lower on highly defended wheat seedling. The experimental switching of the host plants from barley (without chemical defenses) to two wheat species with low and high levels of chemical defenses, revealed that superclone exhibited a flexible probing activities related to access of sieve elements, while the non-superclone exhibited rigid responses. These findings are consistent with the pattern of occurrence of these genotypes in the field on cereals with different plant defenses (e.g. benzoxazinoids). These responses are discussed on the view of developing new strategies for the management in invasive populations of aphid pest species.

Keywords

Sitobion avenaewheatchemical defensesaphid performancesuperclone
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 6 , December 2016 , pp. 801 - 808
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Bernays, E.A. & Funk, D.J. (1999) Specialists make faster decisions than generalists: experiments with aphids. Proceedings of the Royal Society B 266, 151–156.Google Scholar
Caballero, P.P., Ramírez, C.C. & Niemeyer, H.M. (2001) Specialization pattern of the aphid Rhopalosiphum maidis is not modified by experience on a novel host. Entomologia Experimentalis et Applicata 100, 43–52.Google Scholar
Caron, V., Ede, F.J. & Sunnucks, P. (2014) Unravelling the paradox of loss of genetic variation during invasion: superclones may explain the success of a clonal invader. PLoS ONE 9, e97744.CrossRefGoogle ScholarPubMed
Castañeda, L.E., Figueroa, C.C., Fuentes-Contreras, E., Niemeyer, H.M. & Nespolo, R.F. (2009) Energetic costs of detoxification systems in herbivores feeding on chemically defended host plants: a correlational study in the grain aphid, Sitobion avenae . Journal of Experimental Biology 212, 1185–1190.Google Scholar
Castañeda, L.E., Figueroa, C.C., Fuentes-Contreras, E., Niemeyer, H.M. & Nespolo, R.F. (2010 a) Physiological approach to explain the ecological success of ‘superclones’ in aphids: interplay between detoxification enzymes, metabolism and fitness. Journal of Insect Physiology 56, 1058–1064.CrossRefGoogle ScholarPubMed
Castañeda, L.E., Figueroa, C.C. & Nespolo, R.F. (2010 b) Do insect pests perform better on highly defended plants? Costs and benefits of induced detoxification defences in the aphid Sitobion avenae . Journal of Evolutionary Biology 23, 2474–2483.CrossRefGoogle ScholarPubMed
Chen, C.Y., Chiu, M.C. & Kuo, M.H. (2013) Effect of warming with temperature oscillations on a low-latitude aphid, Aphis craccivora . Bulletin of Entomological Research 103(04), 406–413.Google Scholar
Clayton, W.D., Vorontsova, M.S., Harman, K.T. & Williamson, H. (2012) GrassBase-The Online World Grass Flora. Kew, The Board of Trustees, Royal Botanic Gardens, Kew.Google Scholar
De Barro, P.J., Sherratt, T.N., David, O. & Maclean, N. (1995) An investigation of the differential performance of clones of the aphid Sitobion avenae on two host species. Oecologia 104, 379–385.Google Scholar
Dedryver, C.A., Hulle, M., Le Gallic, J.F., Caillaud, M. & Simon, J.C. (2001) Coexistence in space and time of sexual populations of the cereal aphid Sitobion avenae . Oecologia 128, 379–388.Google Scholar
Douglas, A.E. (1997) Provenance, experience and plant utilisation by the polyphagous aphid, Aphis fabae . Entomologia Experimentalis et Applicata 83, 161–170.Google Scholar
Figueroa, C.C., Loayza-Muro, R. & Niemeyer, H.M. (2002) Temporal variation of RAPD-PCR phenotype composition of the grain aphid Sitobion avenae (Hemiptera: Aphididae) on wheat: role of hydroxamic acids. Bulletin of Entomological Research 92, 25–33.Google Scholar
Figueroa, C.C., Simon, J.C., Le Gallic, J.F., Prunier-Leterme, N., Briones, L.M., Dedryver, C.A. & Niemeyer, H.M. (2004) Effect of host defense chemicals on clonal distribution and performance of different genotypes of the cereal aphid Sitobion avenae . Journal of Chemical Ecology 30, 2515–2525.Google Scholar
Figueroa, C.C., Simon, J.C., Le Gallic, J.F., Prunier-Leterme, N., Briones, L.M., Dedryver, C.A. & Niemeyer, H.M. (2005) Genetic structure and clonal diversity of an introduced pest in Chile, the cereal aphid Sitobion avenae . Heredity 95, 24–33.Google Scholar
Forneck, A., Anhalt, U.C.M., Mammerler, R. & Griesser, N. (2015) No evidence of superclones in leaf-feeding forms of austrian grape phylloxera (Daktulosphaira vitifoliae). European Journal of Plant Pathology 142, 441–448.Google Scholar
Gorur, G., Lomonaco, C. & Mackenzie, A. (2005) Phenotypic plasticity in host-plant specialisation in Aphis fabae . Ecological Entomology 30, 657–664.Google Scholar
Gorur, G., Lomonaco, C. & Mackenzie, A. (2007) Phenotypic plasticity in host choice behavior in black bean aphid, Aphis fabae (Homoptera: Aphididae). Arthropod-Plant Interactions 1, 187–194.Google Scholar
Harrison, J.S. & Mondor, E.B. (2011) Evidence for an invasive aphid “Superclone”: extremely low genetic diversity in oleander aphid (Aphis nerii) populations in the Southern United States. PLoS ONE 6, e17524.Google Scholar
Hofman, J. & Hofmanová, O. (1971) 1,4-Benzoxazine derivatives in plants: absence of 2,4-dihydroxy-7-methoxy-2H 1,4-benzoxazin-3/4H/-one from uninjured Zea mays plants. Phytochemistry 10, 1441–1444.CrossRefGoogle Scholar
Hoffmann, A.A., Weeks, A.R., Nash, M., Mangano, G.P. & Umina, P.A. (2008) The changing status of invertebrate pests and the future of pest management in the Australian grains industry. Australian Journal of Experimental Agriculture 48, 1481–1493.Google Scholar
Liu, X.D., Zhai, B.P. & Zhang, X.X. (2008) Specialized host-plant performance of the cotton aphid is altered by experience. Ecological Research 23, 919–925.CrossRefGoogle Scholar
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, 12–34.Google Scholar
Llewellyn, K.S., Loxdale, H.D., Harrington, R., Clark, S.J. & Sunnucks, P. (2004) Evidence for gene flow and local clonal selection in field populations of the grain aphid (Sitobion avenae) in Britain revealed using microsatellites. Heredity 93, 143–153.Google Scholar
Loxdale, H.D., Massonnet, B. & Weisser, W.W. (2010) Why are there so few aphid clones? Bulletin of Entomological Research 100, 613–622.Google Scholar
Lynch, M. (1984) Destabilizing hybridization, general-purpose genotypes and geographic parthenogenesis. The Quarterly Review of Biology 59, 257–290.Google Scholar
Nicol, D., Copaja, S.V., Wratten, S.D. & Niemeyer, H.M. (1992) A screen of worldwide wheat cultivars for Hidroxamic acid levels and aphid antixenosis. Annals of Applied Biology 121, 11–18.Google Scholar
Niemeyer, H.M. (2009) Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. Journal of Agricultural and Food Chemistry 57, 1677–1696.Google Scholar
Olivares-Donoso, R., Troncoso, A.J., Tapia, D.H., Aguilera-Olivares, D. & Niemeyer, H.M. (2007) Contrasting performances of generalist and specialist Myzus persicae (Hemiptera : Aphididae) reveal differential prevalence of maternal effects after host transfer. Bulletin of Entomological Research 97, 61–67.Google Scholar
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.Google Scholar
Prado, E. & Tjallingii, W.F. (1999) Effects of experimental stress factors on probing behaviour by aphids. Entomologia Experimentalis et Applicata 9, 289–300.CrossRefGoogle Scholar
Ramírez, C.C. & Niemeyer, H.M. (2000) The influence of previous experience and starvation on aphid feeding behavior. Journal of Insect Behavior 13, 699–709.Google Scholar
Ramírez, C.C., Caballero, P.P. & Niemeyer, H.M. (1999) Effect of previous exposure to hydroxamic acids in probing behavior of aphid Sitobion fragariae on wheat seedlings. Journal of Chemical Ecology 25, 771–779.CrossRefGoogle Scholar
R-Core T Development Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Sarria, E., Cid, M., Garzo, E. & Fereres, A. (2009) Excel Workbook for automatic parameter calculation of EPG data. Computers and Electronics in Agriculture 67, 35–42.Google Scholar
Simon, J.C., Baumann, S., Sunnucks, P., Hebert, P.D.N., Pierre, J.S., Le Gallic, J.F. & Dedryver, C.A. (1999) Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers. Molecular Ecology 8, 531–545.Google Scholar
Simon, J.C., Rispe, C. & Sunnucks, P. (2002) Ecology and evolution of sex in aphids. Trends in Ecology & Evolution 17(1), 34–39.Google Scholar
StatSoft, Inc. (2004) STATISTICA (data analysis software system), version 7. Available online at www.statsoft.com.Google Scholar
Sunnucks, P., De Barro, P.J., Lushai, G., MacLean, N. & Hales, D. (1997) Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology 6, 1059–1073.Google Scholar
Sunnucks, P., Chisholm, D., Turak, E. & Hales, D.F. (1998) Evolution of an ecological trait in parthenogenetic Sitobion aphids. Heredity 81, 639–647.Google Scholar
Tapia, D.H., Silva, A.X., Ballesteros, G.I., Figueroa, C.C., Niemeyer, H.M. & Ramírez, C.C. (2015) Differences in learning and memory of host plant features between specialist and generalist phytophagous insects. Animal Behavior 106, 1–10.Google Scholar
Tjallingii, W.F. (1990) Continuous recording of stylet penetration activities by aphids. pp. 89–99 in Campbell, R.K. & Raymond, D.E. (Eds) Aphid–Plant Genotype Interactions. Amsterdam, The Netherlands, Elsevier.Google Scholar
Tjallingii, W.F. & Esch, T.H. (1993) Fine-structure of aphid stylet routes in plant-tissues in correlation with EPG signals. Physiological Entomology 18, 317–328.Google Scholar
Vargas, R.R., Troncoso, A.J., Tapia, D.H., Olivares-Donoso, R. & Niemeyer, H.M. (2005) Behavioural differences during host selection between alate virginoparae of generalist and tobacco-specialist Myzus persicae . Entomologia Experimentalis et Applicata 116, 43–53.Google Scholar
Via, S. (1991) Specialized host plant performance of pea aphid clones is not altered by experience. Ecology 72, 1420–1427.Google Scholar
Vorburger, C., Lancaster, M. & Sunnucks, P. (2003) Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two “superclones” in Victoria, Australia. Molecular Ecology 12, 3493–3504.Google Scholar
Webster, B., Qvarfordt, E., Olsson, U. & Glinwood, R. (2013) Different roles for innate and learnt behavioral responses to odors in insect host location. Behavioral Ecology 24, 366–372.Google Scholar
Wilson, A.C.C., Sunnucks, P. & Hales, D.F. (1999) Microevolution, low clonal diversity and genetic affinities of parthenogenetic Sitobion aphids in New Zealand. Molecular Ecology 8, 1655–1666.Google Scholar
Xin, J.J., Shang, Q.L., Desneux, N. & Gao, X.W. (2014) Genetic diversity of Sitobion avenae (Homoptera: Aphididae) populations from different geographic regions in China. PLoS ONE 9, e109349.CrossRefGoogle ScholarPubMed
Zehnder, C.B. & Hunter, M.D. (2009) More is not necessarily better: the impact of limiting and excessive nutrients on herbivore population growth rates. Ecological Entomology 34, 535–543.Google Scholar
Zepeda-Paulo, F.A., Simon, J.C., Ramirez, C.C., Fuentes-Contreras, E., Margaritopoulos, J.T., Wilson, A.C.C. & Figueroa, C.C. (2010) The invasion route for an insect pest species: the tobacco aphid in the New World. Molecular Ecology 19, 4738–4752.Google Scholar