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‘Bottom-up’ effects in a tritrophic plant–aphid–parasitoid system: Why being the perfect host can have its disadvantages

Published online by Cambridge University Press:  10 April 2019

M. Mehrparvar*
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
A. Rajaei
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
M. Rokni
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
A. Balog
Affiliation:
Department of Horticulture, Faculty of Technical and Human Science, Sapientia Hungarian University of Transylvania, Corunca/Sighisoara Str. 1C. Tirgu-Mures, Romania
H.D. Loxdale
Affiliation:
School of Biosciences, Cardiff University, The Sir Martin Evans Building, Museum Avenue, Cardiff, Wales, CF10 3AX, UK
*
*Author for correspondence Phone: 0098 9133400646 Fax: 0098 3433776617 E-mail: mehrparvar@aphidology.com; aphidology@gmail.com

Abstract

In this study the host plant genotype effect on cabbage aphid, Brevicoryne brassicae (L.)(Hemiptera: Aphididae) preference and performance, the effect of aphid genotype on parasitoids performance, as well as the indirect effects of plant genotypes on aphid parasitoid performance, were tested using different population samples of the aphid and its primary endoparasitoid wasp, Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae). Experiments were run as fully-factorial randomized block design in a greenhouse. Accordingly, host plant cultivar had significant effects on the total number of aphids and aphid-load whilst the fitness of the aphid genotypes were also influenced by plant cultivar. The effect of parasitism on cabbage aphids was significantly different between plant cultivars. Overall, the results revealed that cabbage aphid is under different selective pressures arising from both higher (parasitoid) and lower (host plant cultivar) trophic levels. The host plant cultivar had a significant effect on both aphid fitness and parasitism rate on particular aphid genotypes. This indicates that host-plant-adapted aphid species can create much context-dependency in the nature and strength of ‘fitness benefits parasitism’, which may in turn alter the costs and benefits of host specialization.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Balog, A. & Schmitz, O.J. (2013) Predation determines different selective pressure on pea aphid host races in a complex agricultural mosaic. PLoS One 8, e55900.Google Scholar
Benedek, K., Bálint, J., Salamon, R.V., Kovács, E., Ábrahám, B., Fazakas, C., Loxdale, H.D. & Balog, A. (2015) Chemotype of tansy (Tanacetum vulgare L.) determines aphid genotype and its associated predator system. Biological Journal of the Linnean Society 114, 709719.Google Scholar
Berlocher, S.H. & Feder, J.L. (2002) Sympatric speciation in phytophagous insects: moving beyond controversy? Annual Review of Entomology 47, 773815.Google Scholar
Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World's Herbaceous Plants and Shrubs. London, UK, John Wiley & Sons.Google Scholar
Braendle, C., Davis, G.K., Brisson, J.A. & Stern, D.L. (2006) Wing dimorphism in aphids. Heredity 97, 192199.Google Scholar
Brassil, C.E.A.P. (2004) The prevalence of asymmetrical indirect effects in two-host-one-parasitoid systems. Theoretical Population Biology 66, 7182.Google Scholar
Brisson, J.A. (2010) Aphid wing dimorphisms: linking environmental and genetic control of trait variation. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 365, 605616.Google Scholar
Bukovinszky, T., van Veen, F.F., Jongema, Y. & Dicke, M. (2008) Direct and indirect effects of resource quality on food web structure. Science 319, 804807.Google Scholar
Burghardt, K.T. & Schmitz, O.J. (2015) Influence of plant defenses and nutrients on trophic control of ecosystems. pp. 203232 in Hanley, T. & La Pierre, K. (Eds) Trophic ecology: bottom-up and top-down interactions across aquatic and terrestrial systems. Cambridge, Cambridge University Press.Google Scholar
Caillaud, C.M. & Niemeyer, H.M. (1996) Possible involvement of the phloem sealing system in the acceptance of a plant as host by an aphid. Cellular and Molecular Life Sciences 52, 927931.Google Scholar
Davis, A.R., Peterson, R.L. & Shuel, R.W. (1986) Anatomy and vasculature of the floral nectaries of Brassica napus (Brassicaceae). Canadian Journal of Botany 64, 25082516.Google Scholar
Drès, M. & Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 357, 471492.Google Scholar
Eubanks, M.D. & Denno, R.F. (2001) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecological Entomology 25, 140146.Google Scholar
Ferrari, J., Müller, C.B., Kraaijeveld, A.R. & Godfray, H.C.J. (2001) Clonal variation and covariation in aphid resistance to parasitoids and a pathogen. Evolution 55, 18051814.Google Scholar
Futuyma, D.J. & Moreno, G. (1988) The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207233.Google Scholar
Hawlena, D., Kress, H., Dufresne, E.R. & Schmitz, O.J. (2011) Grasshoppers alter jumping biomechanics to enhance escape performance under chronic risk of spider predation. Functional Ecology 25, 279288.Google Scholar
Kunert, G., Belz, E., Simon, J.C., Weisser, W.W. & Outreman, Y. (2010) Differences in defensive behaviour between host-adapted races of the pea aphid. Ecological Entomology 35, 147154.Google Scholar
Loxdale, H.D. (2008) The nature and reality of the aphid clone: genetic variation, adaptation and evolution. Agricultural and Forest Entomology 10, 8190.Google Scholar
Loxdale, H.D. & Balog, A. (2018) Aphid specialism as an example of ecological-evolutionary divergence. Biological Reviews 93, 642657.Google Scholar
Lushai, G., Markovitch, O. & Loxdale, H.D. (2002) Host-based genotype variation in insects revisited. Bulletin of Entomological Research 92, 159164.Google Scholar
Mehrparvar, M., Zytynska, S.E. & Weisser, W.W. (2013) Multiple cues for winged morph production in an aphid metacommunity. PLoS One 8, e58323.Google Scholar
Mehrparvar, M., Mansouri, S.M. & Weisser, W.W. (2014) Mechanisms of species-sorting: effect of habitat occupancy on aphids’ host plant selection. Ecological Entomology 39, 281289.Google Scholar
Mittler, T.E. & Sutherland, O.R.W. (1969) Dietary influences on aphid polymorphism. Entomologia Experimentalis Et Applicata 12, 703713.Google Scholar
Müller, C.B., Williams, I.S. & Hardie, J. (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecological Entomology 26, 330340.Google Scholar
Nosil, P. & Crespi, B.J. (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proceedings of the National Academy of Sciences of the USA 103, 90909095.Google Scholar
Pan, H., Preisser, E.L., Su, Q., Jiao, X., Xie, W., Wang, S., Wu, Q. & Zhang, Y. (2016) Natal host plants can alter herbivore competition. PLoS One 11, e0169142.Google Scholar
Peccoud, J. & Simon, J.C. (2010) The pea aphid complex as a model of ecological speciation. Ecological Entomology 35, 119130.Google Scholar
Relyea, R.A. (2001) The lasting effects of adaptive plasticity: predator-induced tadpoles become long-legged frogs. Ecology 82, 19471955.Google Scholar
Ruiz-Montoya, L., Nunez-Farfan, J. & Vargas, J. (2003) Host-associated genetic structure of Mexican populations of the cabbage aphid Brevicoryne brassicae L. (Homoptera: Aphididae). Heredity 91, 415421.Google Scholar
Schmitz, O.J. (2010) Resolving Ecosystem Complexity. Princeton, Princeton University Press.Google Scholar
van Emden, H.F. & Harrington, R. (Eds) (2007) Aphids As Crop Pests. Wallingford, Oxford, CABI.Google Scholar
van Poecke, R.M.P., Roosjen, M., Pumarino, L. & Dicke, M. (2003) Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species. Entomologia Experimentalis Et Applicata 107, 229236.Google Scholar
van Veen, F.J.F., Morris, R.J. & Godfray, H.C.J. (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annual Review of Entomology 51, 187208.Google Scholar
Walker, M. & Jones, T.H. (2001) Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant–insect herbivore–natural enemy systems. Oikos 93, 177187.Google Scholar
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