Skip to main content
×
Home

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

  • Y. Navasse (a1) (a2), S.A.P. Derocles (a1) (a2), M. Plantegenest (a1) (a2) and A. Le Ralec (a1) (a2)
Abstract
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.

Copyright
Corresponding author
*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
References
Hide All
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, 103112.
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, 242254.
Barahoei H., Madjdzadeh S.M. & Mehrparvar M. (2011) Morphometric differentiation of five biotypes of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae: Aphidiinae) in Iran. Zootaxa 2745, 4352.
Begon M., Townsend C.R. & Harper J.H. (2006) Ecology. From Individuals to Ecosystems. 4th edn. Malden, MA, USA, Blackwell Publishing.
Benton T.G., Vickery J.A. & Wilson J.D. (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecology & Evolution 18, 182188.
Blackman R.L. & Eastop V.F. (2000) Aphids of the World's Crop: An Identification and Information Guide. 2nd edn. Oxford, UK, Wiley-Blackwell.
Blackman R.L. & Eastop V.F. (2006) Aphids on the World's Herbaceous Plants and Shrubs. Chichester, Wiley.
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, 767779.
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, 922932.
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, 39003911.
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.
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, 379391.
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, 925936.
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, 1525.
Dion E., Polin S.E., Simon J.C. & Outreman Y. (2011) Symbiont infection affects aphid defensive behaviours. Biology Letters 7, 743746.
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, 29412950.
Evans D.M., Pocock M.J.O. & Memmott J. (2013) The robustness of a network of ecological networks to habitat loss. Ecology Letters 16, 844852.
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, 25082524.
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, 25152525.
Funk D.J., Filchak K.E. & Feder J.L. (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116, 251267.
Futuyma D.J. (2008) Sympatric speciation: norm or exception. pp. 136148 in Tilmon K. (Ed.) Specialization, Speciation and Radiation: The Evolutionary Biology of Herbivorous Insects. Berkeley, University of California Press.
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.
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, 310.
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, 415421.
Gurr G.M., Wratten S.D. & Luna J.M. (2003) Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology 4, 107116.
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, 689699.
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, 516525.
Højsgaard S. (2004). doBy: groupwise computations of summary statistics. R Package Version, 1.
Holt R.D. & Lawton J.H. (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. American Naturalist 142, 623645.
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, 306340.
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, 181209.
Langer A. & Hance T. (2004) Enhancing parasitism of wheat aphids through apparent competition: a tool for biological control. Agriculture, Ecosystem & Environment 102, 205212.
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, 326332.
Le Guigo P., Rolier A. & Le Corff J. (2012 b) Plant neighborhood influences colonization of Brassicaceae by specialist and generalist aphids. Oecologia 169, 753761.
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, 554565.
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, 363371.
Němec V. & Starý P. (1984) Population diversity of Diaeretiella rapae (M'Int.) (Hym., Aphidiidae), an aphid parasitoid in agroecosystems. Institute of Entomology 97, 223233.
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, 115126.
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, 74957500.
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, 6171.
Pocock M.J.O., Evans D.M. & Memmott J. (2012) The robustness and restoration of a network of ecological networks. Science 335, 973977.
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, 13021310.
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, 137154.
Ravigné V. (2010) La spéciation. pp. 952 in Thomas F., Lefevre T. & Raymond M. Biologie évolutive. 1st edn. Louvain-la-Neuve, Belgium, De Boeck University.
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, 720.
Rehman A. & Powell W. (2010) Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera). Journal of Plant Breeding and Crop Science 2, 299311.
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, 337349.
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, 395400.
Rodriguez M.A. & Hawkins B.A. (2000) Diversity, function and stability in parasitoid communities. Ecology Letters 3, 3540.
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, 6273.
R Development Core Team (2013). R Development Core Team. R: a Language and Environment for Statistical Computing 55, 275286.
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, 11171131.
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, 531545.
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, 136.
Starý P. (2006) Aphid Parasitoids of the Czech Republic. Praha, Czech Republic, Akademie Ved Ceské Republiky.
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, 243248.
Stiling P. & Cornelissen T. (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological Control 34, 236246.
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, 4146.
Thompson J.N. (1994) The Coevolutionary Process. Chicago, University of Chicago Press.
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, 1539.
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, 297307.
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, 552565.
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, 153162.
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, 34563465.
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, 294309.
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, 366374.
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, 477483.
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, 297304.
Wiley E.O. & Lieberman B.S. (2011) Phylogenetic: Theory and Practice of Phylogenetic Systematics. 2nd edn. Hoboken, New Jersey, John Wiley & Sons, Inc.
Wilson B. & Lambdin L. (1987) Suitability of Brevicoryne brassicae and Myzus persicae (Homoptera: Aphididae) as hosts of Diaeretiella rapae (Hymenoptera: Aphidiidae). Entomological News 98, 140146.
Woodward G. & Bohan D. (2013). Ecological Networks in an Agricultural World. Academic Press, vol. 49.
Zhang J., Kapli P. & Stamatakis A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29, 28692876.
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, 223231.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Bulletin of Entomological Research
  • ISSN: 0007-4853
  • EISSN: 1475-2670
  • URL: /core/journals/bulletin-of-entomological-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 5
Total number of PDF views: 27 *
Loading metrics...

Abstract views

Total abstract views: 186 *
Loading metrics...

* Views captured on Cambridge Core between 3rd August 2017 - 22nd November 2017. This data will be updated every 24 hours.