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Multifaceted determinants of host specificity in an aphid parasitoid

  • Behavioral Ecology - Original Paper
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Abstract

The host specificity of insect parasitoids and herbivores is thought to be shaped by a suite of traits that mediate host acceptance and host suitability. We conducted laboratory experiments to identify mechanisms shaping the host specificity of the aphid parasitoid Binodoxys communis. Twenty species of aphids were exposed to B. communis females in microcosms, and detailed observations and rearing studies of 15 of these species were done to determine whether patterns of host use resulted from variation in factors such as host acceptance or variation in host suitability. Six species of aphids exposed to B. communis showed no signs of parasitism. Four of these species were not recognized as hosts and two effectively defended themselves from attack by B. communis. Other aphid species into which parasitoids laid eggs had low suitability as hosts. Parasitoid mortality occurred in the egg or early larval stages for some of these hosts but for others it occurred in late larval stages. Two hypotheses explaining low suitability were investigated in separate experiments: the presence of endosymbiotic bacteria conferring resistance to parasitoids, and aphids feeding on toxic plants. An association between resistance and endosymbiont infection was found in one species (Aphis craccivora), and evidence for the toxic plant hypothesis was found for the milkweed aphids Aphis asclepiadis and Aphis nerii. This research highlights the multifaceted nature of factors determining host specificity in parasitoids.

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References

  • Andow DA, Imura O (1994) Specialization of phytophagous arthropod communities on introduced plants. Ecology 75:296–300

    Article  Google Scholar 

  • Antolin MF, Bjorksten TA, Vaughn TT (2006) Host-related fitness trade-offs in a presumed generalist parasitoid, Diaeretiella rapae (Hymenoptera: Aphidiidae). Ecol Entomol 31:242–254

    Article  Google Scholar 

  • Askew RR (1994) Parasitoids of leaf-mining Lepidoptera: what determines their host ranges? In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 177–202

    Google Scholar 

  • Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187. doi:10.1146/annurev.ento.54.110807.090537

    Google Scholar 

  • Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide. Wiley, Chichester

    Google Scholar 

  • Blackman RL, Eastop VF (2006) Aphids on the world’s herbaceous plants and shrubs. Wiley, Chichester

    Google Scholar 

  • Brodeur J, Geervliet JBF, Vet LEM (1996) The role of host species, age and defensive behaviour on ovipositional decisions in a solitary specialist and gregarious generalist parasitoid (Cotesia species). Entomol Exp Appl 81:125–132

    Article  Google Scholar 

  • Chau A, Mackauer M (2001) Preference of the aphid parasitoid Monoctonus paulensis (Hymenoptera: Braconidae, Aphidiinae) for different aphid species: female choice and offspring survival. Biol Control 20:30–38

    Article  Google Scholar 

  • Chen JH, Shi QX (2001) Systematic studies of Aphidiidae of China (Hymenoptera: Aphidiidae). Huayu Nature Book Trade, Fujian

    Google Scholar 

  • Coeur d’Acier A, Jousselin E, Martin JF, Rasplus JY (2007) Phylogeny of the genus Aphis Linnaeus, 1758 (Homoptera: Aphididae) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 42:598–611

    Article  PubMed  Google Scholar 

  • De Farias AMI, Hopper KR (1999) Oviposition behavior of Aphelinus asychis (Hymenoptera: Aphelinidae) and Aphidius matricariae (Hymenoptera: Aphidiidae) and defense behavior of their host Diuraphis noxia (Homoptera: Aphididae). Environ Entomol 28:858–862

    Google Scholar 

  • Desneux N, Barta RJ, Delebecque CJ, Heimpel GE (2009) Transient host paralysis as a means of reducing self-superparasitism in koinobiont endoparasitoids. J Insect Physiol. doi:10.1016/j.jinsphys.2008.12.009

  • Driessen G, Hemerik L, Boonstra B (1991) Host selection behaviour of the parasitoid Leptopilina clavipes in relation to survival in hosts. Neth J Zool 41:99–111

    Article  Google Scholar 

  • Falabella P, Tremblay E, Pennacchio F (2000) Host regulation by the aphid parasitoid Aphidius ervi: the role of teratocytes. Entomol Exp Appl 97:1–9

    Article  Google Scholar 

  • Fuentes-Contreras JE, Powell W, Wadhams LJ, Pickett JA, Niemeyer HM (1996) Influence of wheat and oat cultivars on the development of the cereal aphid parasitoid Aphidius rhopalosiphi and the generalist aphid parasitoid Ephedrus plagiator. Ann Appl Biol 129:181–187

    Article  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gardner SM, Dixon AFG (1985) Plant structure and the foraging success of Aphidius rhopalosiphi (Hymenoptera, Aphidiidae). Ecol Entomol 10:171–179

    Article  Google Scholar 

  • Gerling D, Roitberg BD, Mackauer M (1990) Instarspecific defense of the pea aphid, Acyrthosiphon pisum—influence on oviposition success of the parasite Aphelinus asychis (Hymenoptera, Aphelinidae). J Insect Behav 3:501–514

    Article  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioural and evolutionary ecology. Princeton University Press, Chichester

    Google Scholar 

  • Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Annu Rev Entomol 38:251–273

    Article  Google Scholar 

  • Heimpel GE, Lundgren JG (2000) Sex ratios of commercially reared biological control agents. Biol Control 19:77–93

    Article  Google Scholar 

  • Heimpel GE, Neuhauser C, Hoogendoorn M (2003) Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecol Lett 6:556–566

    Article  Google Scholar 

  • Helms SE, Connelly SJ, Hunter MD (2004) Effects of variation among plant species on the interaction between a herbivore and its parasitoid. Ecol Entomol 29:44–51

    Article  Google Scholar 

  • Henry LM, Roitberg BD, Gillespie DR (2006) Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour. Proc R Soc Lond B Biol 273:2893–2899

    Article  Google Scholar 

  • Hull-Sanders HM, Eubanks MD (2005) Plant defense theory provides insight into interactions involving inbred plants and insect herbivores. Ecology 86:897–904

    Article  Google Scholar 

  • Jaenike J (1978) On optimal oviposition behavior in phytophagous insects. Theor Popul Biol 14:350–356

    Article  PubMed  CAS  Google Scholar 

  • Janssen A (1989) Optimal host selection by Drosophila parasitoids in the field. Funct Ecol 3:469–479

    Article  Google Scholar 

  • Jervis MA, Ellers J, Harvey JA (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu Rev Entomol 53:361–385

    Article  PubMed  CAS  Google Scholar 

  • Kraaijeveld AR, Nowee B, Najem RW (1995) Adaptive variation in host-selection behaviour of Asobara tabida, a parasitoid of Drosophila larvae. Funct Ecol 9:113–118

    Article  Google Scholar 

  • Malcolm SB (1989) Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J Chem Ecol 15:1699–1716

    Article  CAS  Google Scholar 

  • Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol Exp Appl 80:193–196

    Article  CAS  Google Scholar 

  • Martel JW, Malcolm SB (2004) Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. J Chem Ecol 30:545–561

    Article  PubMed  CAS  Google Scholar 

  • Martos A, Givovich A, Niemeyer HM (1992) Effect of DIMBOA, an aphid resistance factor in wheat, on the aphid predator Eriopis connexa Germar (Coleoptera, Coccinellidae). J Chem Ecol 18:469–479

    Article  CAS  Google Scholar 

  • Memmott J, Godfray HCJ, Gauld JD (1994) The structure of a tropical host parasitoid community. J Anim Ecol 63:521–540

    Article  Google Scholar 

  • Mooney KA, Jones P, Agrawal AA (2008) Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids. Oikos 117:450–458

    Article  CAS  Google Scholar 

  • Morehead SA, Feener DH Jr (2000) An experimental test of potential host range in the ant parasitoid Apocephalus paraponerae. Ecol Entomol 25:332–340

    Article  Google Scholar 

  • Novotny V, Miller SE, Cizek L, Leps J, Janda M, Basset Y, Weiblen GD, Darrow K (2003) Colonising aliens: caterpillars (Lepidoptera) feeding on Piper aduncum and P. umbellatum in rainforests of Papua New Guinea. Ecol Entomol 28:704–716

    Article  Google Scholar 

  • Ode PJ (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185

    Article  PubMed  CAS  Google Scholar 

  • Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    Article  PubMed  CAS  Google Scholar 

  • Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800

    Article  PubMed  CAS  Google Scholar 

  • Pasteels JM (1978) Apterous and brachypterous coccinellids at the end of the food chain, Cionura erecta (Asclepiadaceae)—Aphis nerii. Entomol Exp Appl 24:379–384

    Article  Google Scholar 

  • Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic hymenoptera. Annu Rev Entomol 51:233–258

    Article  PubMed  CAS  Google Scholar 

  • Pennacchio F, Fanti P, Falabella P, Digilio MC, Bisaccia F, Tremblay E (1999) Development and nutrition of the Braconid wasp, Aphidius ervi in aposymbiotic host aphids. Arch Insect Biochem 40:53–63

    Article  CAS  Google Scholar 

  • Pratt C, Pope TW, Powell G, Rossiter JT (2008) Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two coccinellid species. J Chem Ecol 34:323–329

    Article  PubMed  CAS  Google Scholar 

  • Rahbé Y, Digilio MC, Febvay G, Guillaud J, Fanti P, Pennacchio F (2002) Metabolic and symbiotic interactions in amino acid pools of the pea aphid, Acyrthosiphon pisum, parasitized by the braconid Aphidius ervi. J Insect Physiol 48:507–516

    Article  PubMed  Google Scholar 

  • Rothschild M, von Euw J, Reichstein T (1970) Cardiac glycosides in oleander Aphid, Aphis nerii. J Insect Physiol 16:1141–1145

    Article  PubMed  CAS  Google Scholar 

  • Russell JA, Latorre A, Sabater-Munoz B, Moya A, Moran NA (2003) Side-stepping secondary symbionts: widespread horizontal transfer across and beyond the Aphidoidea. Mol Ecol 12:1061–1075

    Article  PubMed  CAS  Google Scholar 

  • Schadel WE, Walter WM Jr (1981) Localization of phenols and polyphenol oxidase in ‘Jewel’ sweet potatoes (Ipomoea batatas ‘Jewel’). Can J Bot 59:1961–1967

    CAS  Google Scholar 

  • Shaw MR (1994) Parasitoid host ranges. In: Hawkins BA, Sheehan W (eds) Parasitoid community ecology. Oxford University Press, Oxford, pp 111–144

    Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Stireman JO, Nason JD, Heard SB, Seehawer JM (2006) Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc R Soc Lond B Biol 273:523–530

    Article  CAS  Google Scholar 

  • Takada H (2002) Parasitoids (Hymenoptera: Braconidae, Aphidiinae; Aphelinidae) of four principal pest aphids (Homoptera: Aphididae) on greenhouse vegetable crops in Japan. Appl Entomol Zool 37:237–249

    Article  Google Scholar 

  • van Alphen JJM, Vet LEM (1986) An evolutionary approach to host finding and selection. In: Waage J, Greathead D (eds) Insect parasitoids. Academic Press, London, pp 23–61

    Google Scholar 

  • Völkl W, Kroupa AS (1997) Effects of adult mortality risks on parasitoid foraging tactics. Anim Behav 54:349–359

    Article  Google Scholar 

  • von Dohlen CD, Rowe CA, Heie OE (2006) A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Mol Phylogenet Evol 38:316–329

    Article  Google Scholar 

  • Warashina T, Noro T (2000) Cardenolide and oxypregnane glycosides from the root of Asclepias incarnata L. Chem Pharm Bull 48:516–524

    PubMed  CAS  Google Scholar 

  • Wyckhuys KAG, Hopper KR, Wu KM, Straub C, Cratton C, Heimpel GE (2007a) Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News Inf 28:30N–34N

    Google Scholar 

  • Wyckhuys KAG, Koch RL, Heimpel GE (2007b) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biol Control 40:306–313

    Article  Google Scholar 

  • Wyckhuys KAG, Stone L, Desneux N, Hoelmer KA, Hopper KR, Heimpel GE (2008) Parasitism of the soybean aphid Aphis glycines by Binodoxys communis: the role of aphid defensive behavior and parasitoid reproductive performance. Bull Entomol Res 98:361–370

    Article  PubMed  CAS  Google Scholar 

  • Wyckhuys KAG, Koch RL, Kula RR, Heimpel GE (2009) Potential exposure of a classical biological control agent of the soybean aphid, Aphis glycines, on non-target aphids in North America. Biol Invasions. doi: 10.1007/s10530-008-9299-x

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Acknowledgements

We thank Jacques Brodeur, Martha Hunter, Zeynep Sezen for comments on the manuscript, and Nancy Fares, Burke Bourne and Edwige Desneux for technical assistance. This work was funded in part by a USDA-RAMP project, in part by the North Central Soybean Research Council, and in part by the Minnesota Agricultural Experiment Station.

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Authors and Affiliations

  1. Department of Entomology, University of Minnesota, 1980 Folwell Avenue, Saint Paul, MN, 55108, USA

    Nicolas Desneux, Ruth J. Barta & George E. Heimpel

  2. Beneficial Insect Introductions Research Unit, USDA-ARS, 501 South Chapel Street, Newark, DE, 19713, USA

    Kim A. Hoelmer & Keith R. Hopper

  3. Unité de Recherches Intégrées en Horticulture, INRA, 400 route des chappes, 06903, Sophia-Antipolis, France

    Nicolas Desneux

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  1. Nicolas Desneux
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  2. Ruth J. Barta
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  5. George E. Heimpel
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Correspondence to Nicolas Desneux.

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Communicated by Bernhard Stadler.

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Desneux, N., Barta, R.J., Hoelmer, K.A. et al. Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160, 387–398 (2009). https://doi.org/10.1007/s00442-009-1289-x

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  • DOI: https://doi.org/10.1007/s00442-009-1289-x

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