Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-05-12T09:12:32.771Z Has data issue: false hasContentIssue false
  • English
  • Français

Ecological specialization in Diaeretiella rapae (Hymenoptera: Braconidae: Aphidiinae) on aphid species from wild and cultivated plants

Published online by Cambridge University Press:  03 August 2017

Y. Navasse ,
S.A.P. Derocles ,
M. Plantegenest  and
A. Le Ralec
Y. Navasse
Affiliation:
INRA-Agrocampus Ouest-Université de Rennes 1, UMR1349 IGEPP, 65 rue de Saint-Brieuc, CS 84215, 35 042 Rennes Cedex, France Université Bretagne Loire, Rennes, France
S.A.P. Derocles
Affiliation:
INRA-Agrocampus Ouest-Université de Rennes 1, UMR1349 IGEPP, 65 rue de Saint-Brieuc, CS 84215, 35 042 Rennes Cedex, France Université Bretagne Loire, Rennes, France
M. Plantegenest
Affiliation:
INRA-Agrocampus Ouest-Université de Rennes 1, UMR1349 IGEPP, 65 rue de Saint-Brieuc, CS 84215, 35 042 Rennes Cedex, France Université Bretagne Loire, Rennes, France
A. Le Ralec*
Affiliation:
INRA-Agrocampus Ouest-Université de Rennes 1, UMR1349 IGEPP, 65 rue de Saint-Brieuc, CS 84215, 35 042 Rennes Cedex, France Université Bretagne Loire, Rennes, France
*
*Author for correspondence: Phone: +33 (0)2 23 48 56 74 Fax: +33 (0)2 23 48 54 71 E-mail: anne.leralec@agrocampus-ouest.fr
Get access Rights & Permissions [Opens in a new window]

Abstract

Diaeretiella rapae is an aphid parasitoid with potential for use in biological control strategies. However, several recent genetic studies have challenged the long held view that it is a generalist parasitoid. We investigated its ecological specialization and ability to use resources in cultivated and uncultivated areas. Ecological specialization would reduce its ability to exploit the diversity of aphid species, particularly in uncultivated areas, and to control pest aphids. Four D. rapae strains were studied, three reared on pest aphids on Brassicaceae and one strain on a non-pest aphid on Chenopodiaceae. For each strain, we performed host-switching experiments, with a total of six aphid species, five of which D. rapae parasitizes in France. We tested cross-breeding ability between strains to detect potential reproductive isolation linked to aphid host species in D. rapae. The strain reared on non-pest aphids was able to develop on aphid species from both cultivated and uncultivated plants. The strains reared on pest aphids, however, exclusively parasitized aphid species on cultivated Brassicaceae. In addition, reproductive isolation was detected between strains from uncultivated and cultivated plants. Thus, the D. rapae populations examined here appear to be showing ecological specialization or they may even be composed of a complex of cryptic species related to the aphid hosts. The role of Chenopodium album as a reservoir for D. rapae, by providing a habitat for non-pest aphids on which it can feed, appears to be severely limited, and thus its efficiency to maintain local populations of D. rapae in the vicinity of crops is questionable.

Keywords

host rangehost switchingreproductive isolationnon-cultivated areasagroecosystemBrevicoryne brassicaeHayhurstia atriplicis
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 2 , April 2018 , pp. 175 - 184
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Alhmedi, A., Haubruge, E., D'Hoedt, S. & Francis, F. (2011) Quantitative food webs of herbivore and related beneficial community in non- crop and crop habitats. Biological Control 58, 103–112.Google Scholar
Antolin, M.F., Bjorksten, T.A. & Vaughn, T.T. (2006) Host-related fitness trade-offs in a presumed generalist parasitoid, Diaeretiella rapae (Hymenoptera: Aphidiidae). Ecological Entomology 31, 242–254.CrossRefGoogle Scholar
Barahoei, H., Madjdzadeh, S.M. & Mehrparvar, M. (2011) Morphometric differentiation of five biotypes of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) in Iran. Zootaxa 2745, 43–52.Google Scholar
Begon, M., Townsend, C.R. & Harper, J.H. (2006) Ecology. From Individuals to Ecosystems. 4th edn. Malden, MA, USA, Blackwell Publishing.Google Scholar
Benton, T.G., Vickery, J.A. & Wilson, J.D. (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecology & Evolution 18, 182–188.CrossRefGoogle Scholar
Blackman, R.L. & Eastop, V.F. (2000) Aphids of the World's Crop: An Identification and Information Guide. 2nd edn. Oxford, UK, Wiley-Blackwell.Google Scholar
Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World's Herbaceous Plants and Shrubs. Chichester, Wiley.Google Scholar
Blande, J.D., Pickett, J.A. & Poppy, G.M. (2007) A comparison of semiochemically mediated interactions involving specialist and generalist Brassica-feeding aphids and the braconid parasitoid Diaeretiella rapae . Journal of Chemical Ecology 33, 767–779.Google Scholar
Chaplin-Kramer, R., O'Rourke, E., Blitzer, E.J. & Kremen, C. (2011) A meta-analysis of crop pest and natural enemy response to landscape complexity. Ecology Letters 14, 922–932.Google Scholar
Derocles, S.A.P., Le Ralec, A., Besson, M.M., Maret, M., Walton, A., Evans, D.M. & Plantegenest, M. (2014) Molecular analysis reveals high compartmentalisation in aphid-primary parasitoid networks and low parasitoid sharing between crop and non-crop habitats. Molecular Ecology 23, 3900–3911.Google Scholar
Derocles, S.A.P., Evans, D.M., Nichols, P.C., Evans, S.A. & Lunt, D.H. (2015). Determining plant–leaf miner–parasitoid interactions: a DNA barcoding approach. PLoS ONE 10, e0117872.Google Scholar
Derocles, S.A.P., Plantegenest, M., Rasplus, J.Y., Marie, A., Evans, D.M., Lunt, D.H. & Le Ralec, A. (2016) Are generalist Aphidiinae (Hym. Braconidae) mostly cryptic species complexes? Systematic Entomology 41, 379–391.Google Scholar
Desneux, N., Starý, P., Delebecque, C.J., Gariepy, T.D., Barta, R.J., Hoelmer, K.A. & Heimpel, G.E. (2009) Cryptic species of parasitoids attacking the Soybean Aphid (Hemiptera: Aphididae) in Asia: Binodoxys communis and Binodoxys koreanus (Hymenoptera: Braconidae: Aphidiinae). Annals of the Entomological Society of America 102, 925–936.Google Scholar
Devictor, V., Clavel, J., Julliard, R., Lavergne, S., Mouillot, D., Thuiller, W., Venail, P., Villeger, S. & Mouquet, N. (2010) Defining and measuring ecological specialization. Journal of Applied Entomology 47, 15–25.Google Scholar
Dion, E., Polin, S.E., Simon, J.C. & Outreman, Y. (2011) Symbiont infection affects aphid defensive behaviours. Biology Letters 7, 743–746.Google Scholar
Evans, D.M., Pocock, M.J.O., Brooks, J. & Memmott, J. (2011) Seeds in farmland food-webs: resource importance, distribution and the impacts of farm management. Biological Conservation 144, 2941–2950.CrossRefGoogle Scholar
Evans, D.M., Pocock, M.J.O. & Memmott, J. (2013) The robustness of a network of ecological networks to habitat loss. Ecology Letters 16, 844–852.Google Scholar
Ferrari, J., Via, S. & Godfray, H.C.J. (2008) Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 62, 2508–2524.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
Funk, D.J., Filchak, K.E. & Feder, J.L. (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116, 251–267.Google Scholar
Futuyma, D.J. (2008) Sympatric speciation: norm or exception. pp. 136–148 in Tilmon, K. (Ed.) Specialization, Speciation and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, University of California Press.Google Scholar
Gagic, V., Petrović-Obradović, O., Fründ, J., Kavallieratos, N.G., Athanassiou, C.G., Starý, P. & Tomanović, Ž. (2016) The effects of aphid traits on parasitoid host use and specialist advantage. PLoS ONE 11, e0157674.CrossRefGoogle ScholarPubMed
Godfray, H.C.J. & Shimada, M. (1999) Parasitoids: a model system to answer questions in behavioral, evolutionary and population ecology. Researches on Population Ecology 41, 3–10.Google Scholar
Guerrieri, E., Pennacchio, F. & Tremblay, E. (1993) Flight behaviour of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae) in response to plant and host volatiles. European Journal of Entomology 90, 415–421.Google Scholar
Gurr, G.M., Wratten, S.D. & Luna, J.M. (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology 4, 107–116.CrossRefGoogle Scholar
Henry, L.M., Roitberg, B.D. & Gillespie, D.R. (2008) Host-range evolution in Aphidius parasitoids: fidelity, virulence and fitness trade-offs on an ancestral host. Evolution 62, 689–699.Google Scholar
Henry, L.M., Maiden, M.C., Ferrari, J. & Godfray, H.C.J. (2015) Insect life history and the evolution of bacterial mutualism. Ecology letters 18, 516–525.Google Scholar
Højsgaard, S. (2004). doBy: groupwise computations of summary statistics. R Package Version, 1.Google Scholar
Holt, R.D. & Lawton, J.H. (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. American Naturalist 142, 623–645.CrossRefGoogle ScholarPubMed
Kavallieratos, N.G., Lykouressis, D.P., Sarlis, G.P., Stathas, G.J., Segovia, A.S. & Athanassiou, C.G. (2001) The Aphidiinae (Hymenoptera: Ichneumonoidea: Braconidae) of Greece. Phytoparasitica 29, 306–340.Google Scholar
Kavallieratos, N.G., Tomanović, Ž., Starý, P., Athanassiou, C.G., Fasseas, C., Petrović, O., Niketić, O., Stanisavljević, L.Z. & Veroniki, M.A. (2005) Praon Haliday (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe: key, host range and phylogenetic relationships. Zoologischer Anzeiger 243, 181–209.Google Scholar
Langer, A. & Hance, T. (2004) Enhancing parasitism of wheat aphids through apparent competition: a tool for biological control. Agriculture, Ecosystem & Environment 102, 205–212.CrossRefGoogle Scholar
Le Guigo, P., Maingeneau, A. & Le Corff, J. (2012 a) Performance of an aphid Myzus persicae and its parasitoid Diaeretiella rapae on wild and cultivated Brassicae. Journal of Plant Interaction 7, 326–332.CrossRefGoogle Scholar
Le Guigo, P., Rolier, A. & Le Corff, J. (2012 b) Plant neighborhood influences colonization of Brassicaceae by specialist and generalist aphids. Oecologia 169, 753–761.CrossRefGoogle ScholarPubMed
Le Ralec, A., Anselme, C., Outreman, Y., Poirié, M., Van Baaren, J., Le Lann, C. & Jacques, J. M. (2010) Evolutionary ecology of the interactions between aphids and their parasitoids. Comptes Rendus Biologies 333, 554–565.Google Scholar
Le Ralec, A., Ribule, A., Barragan, A. & Outreman, Y. (2011) Host range limitation caused by incomplete host regulation in an aphid parasitoid. Journal of Insect Physiology 57, 363–371.Google Scholar
Němec, V. & Starý, P. (1984) Population diversity of Diaeretiella rapae (M'Int.) (Hym., Aphidiidae), an aphid parasitoid in agroecosystems. Institute of Entomology 97, 223–233.Google Scholar
Neuville, S., Le Ralec, A., Outreman, Y. & Jaloux, B. (2016) The delay in arrival of the parasitoid Diaeretiella rapae influences the efficiency of cabbage aphid biological control. Biological Control 61, 115–126.Google Scholar
Peccoud, J., Ollivier, A., Plantegenest, M. & Simon, J.C. (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences of the United States of America 106, 7495–7500.Google Scholar
Pike, K., Starý, P., Miller, T., Allison, D., Graf, L., Boydston, R., Miller, R. & Gillespsie, R. (1999) Host range and habitats of the Aphid parasitoid Diaeretiella rapae (Hymenoptera: Aphidiidae) in Washington State. Environmental Entomologia 28, 61–71.Google Scholar
Pocock, M.J.O., Evans, D.M. & Memmott, J. (2012) The robustness and restoration of a network of ecological networks. Science 335, 973–977.Google Scholar
Pope, T.W., Kissen, R., Grant, M., Pickett, J.A., Rossiter, J.T. & Powell, G. (2008) Comparative innate responses of the aphid parasitoid Diaeretiella rapae to alkenyl glucosinolate derived isothiocyanates, nitriles, and epithionitriles. Journal of Chemical Ecology 34, 1302–1310.Google Scholar
Pyke, G.H.P, Pulliam, H.R. & Charnov, E.L. (1977) Optimal foraging: a selective review of theory and tests. Quarterly Review of Biology 52, 137–154.Google Scholar
Ravigné, V. (2010) La spéciation. pp. 9–52 in Thomas, F., Lefevre, T. & Raymond, M. Biologie évolutive. 1st edn. Louvain-la-Neuve, Belgium, De Boeck University.Google Scholar
Raymond, L., Plantegenest, M., Gagic, V., Navasse, Y. & Lavandero, B. (2016). Aphid parasitoid generalism: development, assessment, and implications for biocontrol. Journal of Pest Science 89, 7–20.Google Scholar
Rehman, A. & Powell, W. (2010) Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera). Journal of Plant Breeding and Crop Science 2, 299–311.Google Scholar
Ricci, B., Franck, P., Toubon, J.F., Bouvier, J.C., Sauphanor, B. & Lavigne, C. (2009) The influence of landscape on insect pest dynamics: a case study in southeastern France. Landscape Ecology 24, 337–349.Google Scholar
Ricci, B., Franck, P., Bouvier, J.C., Casado, D. & Lavigne, C. (2011) Effects of hedgerow characteristics on intra-orchard distribution of larval codling moth. Agriculture, Ecosystems & Environment 140, 395–400.CrossRefGoogle Scholar
Rodriguez, M.A. & Hawkins, B.A. (2000) Diversity, function and stability in parasitoid communities. Ecology Letters 3, 35–40.Google Scholar
Rusch, A., Valantin-Morison, M., Roger-Estrade, J. & Sarthou, J.P. (2012) Using landscape indicators to predict high pest infestations and successful natural pest control at the regional scale. Landscape and Urban Planning 105, 62–73.Google Scholar
R Development Core Team (2013). R Development Core Team. R: a Language and Environment for Statistical Computing 55, 275–286.Google Scholar
Sanchis, A., Michelena, J.M., Latorre, A., Quicke, D.L.J., Gardenfors, U. & Belshaw, R. (2001) The phylogenetic analysis of variable-length sequence data: elongation factor-1a introns in European populations of the parasitoid wasp genus Pauesia (Hymenoptera: Braconidae: Aphidiinae). Molecular Ecology Resources 18, 1117–1131.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
Singh, R. & Singh, G. (2015) Systematics, distribution and host range of Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae, Aphidiinae). International Journal of Research Studies in Biosciences 3, 1–36.Google Scholar
Starý, P. (2006) Aphid Parasitoids of the Czech Republic. Praha, Czech Republic, Akademie Ved Ceské Republiky.Google Scholar
Starý, P. & González, D. (1991) The Chenopodium aphid, Hayhurstia atriplicis (L.) (Hym., Aphididae), a parasitoid reservoir and a source of biocontrol agents in pest management. Journal of Applied Entomology 111, 243–248.Google Scholar
Stiling, P. & Cornelissen, T. (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological Control 34, 236–246.Google Scholar
Storeck, A., Poppy, G., Van Emden, H.F. & Powell, W. (2000) The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani . Entomologia Experimentalis et Applicata 97, 41–46.Google Scholar
Thompson, J.N. (1994) The Coevolutionary Process. Chicago, University of Chicago Press.Google Scholar
Tomanović, Ž., Kavallieratos, N.G., Starý, P., Athanassiou, C.G., Žikić, V., Petrović-Obradović, O. & Sarlis, G.P. (2003) Aphidius Nees aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) in Serbia and Montenegro: tritrophic associations and key. Acta Entomologica Serbica 8, 15–39.Google Scholar
Tomanović, Ž., Rakhshani, E., Starý, P., Kavallieratos, N.G., Stanisavljević, L.Z., Žikić, V. & Athanassiou, C.G. (2007) Phylogenetic relationships between the genera Aphidius and Lysaphidus (Hym. Braconidae: Aphidiinae) with description of Aphidius iranicus sp nov. Canadian Entomologist 139, 297–307.Google Scholar
Tomanović, Ž., Petrović, A., Mitrović, M., Kavallieratos, N.G., Starý, P., Rakhshani, E., Rakhshanipour, M., Popović, A., Shukshuk, A.H. & Ivanović, A. (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bulletin of Entomological Research 104, 552–565.Google Scholar
Tomić, M., Tomanović, Ž., Kavallieratos, N.G., Starý, P., Athanassioud, C.G., Tomić, V. & Lucic, L. (2005) Morphological variability of several biotypes of Ephedrus plagiator (Nees, 1811) (Hymenoptera: Braconidae: Aphidiinae) and description of a new species. Zoologischer Anzeiger 244, 153–162.Google Scholar
Toneatto, F., Nielsen, J.K., Ørgaard, M. & Hauser, T.P. (2010) Genetic and sexual separation between insect resistant and susceptible Barbarea vulgaris plants in Denmark. Molecular Ecology 19, 3456–3465.CrossRefGoogle ScholarPubMed
Tscharntke, T., Bommarco, R., Clough, Y., Crist, T.O., Kleijn, D., Rand, T.A., Tylianakis, J.M., van Nouhuys, S. & Vidal, S. (2007) Conservation biological control and enemy diversity on a landscape scale. Biological Control 43, 294–309.Google Scholar
Vafaie, E.K., Fitzpatrick, S.M. & Cory, J.S. (2013) Does rearing an aphid parasitoid on one host affect its ability to parasitize another species? Agricultural and Forest Entomology 15, 366–374.Google Scholar
Van Emden, H.F., Storeck, A.P., Douloumpaka, S., Eleftherianos, I., Poppy, G.M. & Powell, W. (2008) Plant chemistry and aphid parasitoids (Hymenoptera: Braconidae): imprinting and memory. European Journal of Entomology 105, 477–483.Google Scholar
Wickremasinghe, M.G.V. & Van Emden, H.F. (1992) Reactions of adult female parasitoids, particularly Aphidius rhopalosiphi, to volatile chemical cues from the host plants of their aphid prey. Physiological Entomology 17, 297–304.Google Scholar
Wiley, E.O. & Lieberman, B.S. (2011) Phylogenetic: Theory and Practice of Phylogenetic Systematics. 2nd edn. Hoboken, New Jersey, John Wiley & Sons, Inc.CrossRefGoogle Scholar
Wilson, B. & Lambdin, L. (1987) Suitability of Brevicoryne brassicae and Myzus persicae (Homoptera: Aphididae) as hosts of Diaeretiella rapae (Hymenoptera: Aphidiidae). Entomological News 98, 140–146.Google Scholar
Woodward, G. & Bohan, D. (2013). Ecological Networks in an Agricultural World. Academic Press, vol. 49.Google Scholar
Zhang, J., Kapli, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 2869–2876.Google Scholar
Žikić, V., Tomanović, Ž., Ivanovic, A., Kavallieratos, N.G., Starý, P., Stanisavljevic, L.Z. & Rakhshani, E. (2009) Morphological characterization of Ephedrus persicae biotypes (Hymenoptera: Braconidae: Aphidiinae) in the Palaeartic. Annals of the Entomological Society of America 102, 223–231.Google Scholar