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Host specialization of parasitoids and their hyperparasitoids on a pair of syntopic aphid species

Published online by Cambridge University Press:  13 March 2013

Sämi Schär*
Affiliation:
Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zürich, Switzerland
Christoph Vorburger
Affiliation:
Institute of Integrative Biology, ETH Zürich, Switzerland EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600 Dübendorf, Switzerland
*
*Author for correspondence Phone: +45 353-21238 Fax: +45 353-21250 E-mail: SSchar@bio.ku.dk, saemi.schaer@gmail.com

Abstract

Parasitoids of herbivorous insects have frequently evolved specialized lineages exploiting hosts occurring on different plants. This study investigated whether host specialization is also observed when closely related parasitoids exploit herbivorous hosts sharing the same host plant. The question was addressed in economically relevant aphid parasitoids of the Lysiphlebus fabarum group. They exploit two aphid species (Aphis fabae cirsiiacanthoides and Brachycaudus cardui), co-occurring in mixed colonies (syntopy) on the spear thistle (Cirsium vulgare). Two morphologically distinguishable parasitoid lineages of the genus Lysiphlebus were observed and each showed virtually perfect host specialization on one of the two aphid species in this system. From A. f. cirsiiacanthoides, only females emerged that morphologically belonged to Lysiphlebus cardui, while males and females belonging to L. fabarum hatched from B. cardui. Microsatellite analyses indicated clear genetic differentiation of L. fabarum and L. cardui. L. cardui comprised only two distinct asexual lineages, one of which predominated throughout the area investigated. Population genetic analysis of sexual L. fabarum showed evidence for relatively strong spatial structuring and limited dispersal ability. Hyperparasitoids emerged from a large proportion of aphid mummies. One species, Pachyneuron aphidis, was significantly associated with B. cardui/L. fabarum mummies, indicating that host specialization may even extend to the trophic level above parasitoids.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

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References

Andrews, F.G. (1978) Taxonomy and Host Specificity of Nearctic Alloxystinae: With a Catalog of the World Species (Hymenoptera: Cynipidae). State of California, Department of food and agriculture, Division of plant industry, Laboratory services.Google Scholar
Arnaud-Haond, S. & Belkhir, K. (2007) Genclone: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7, 1517.Google Scholar
Belshaw, R., Quicke, D.L.J., Völkl, W. & Godfray, H.C.J. (1999) Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Evolution 53, 11891199.CrossRefGoogle 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. (2000) Aphids on the World's Crops: An Identification and Information Guide. 2nd edn. Chichester, John Wiley and Sons.Google Scholar
Bush, G.L. (1969) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution 23, 237251.CrossRefGoogle Scholar
Cavalli-Sforza, L.L. & Edwards, A.W.F. (1967) Phylogenetic analysis: models and estimation procedures. American Journal of Human Genetics 19 (3, Part I), 233257.Google Scholar
Craig, T.P., Horner, J.D. & Itami, J.K. (1997) Hybridization studies on the host races of Eurosta solidaginis: implications for sympatric speciation. Evolution 51, 15521560.Google Scholar
de Vere Graham, M.W.R. (1969) The Pteromalidae of North-western Europe (Hymenoptera: Chalcidoidea). Supplement 16, London, Bulletin of the British Museum (Natural History).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
Earl, D.A. & vonHolt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources. 4, 359361. Available online at taylor0.biology.ucla.edu/structureHarvester/.Google Scholar
Erdös, J. (1964) Chalcidoidea III. in Fauna Hung. 73. Budapest, Akademiaikiado Budapest.Google Scholar
Ersts, P.J. (2007) Geographic distance matrix generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. Available online at http://biodiversityinformatics.amnh.org/open_source/gdmg.Google Scholar
Evenhuis, H.H. & Kiriak, I.G. (1985) Studies on Alloxystidae (Hymenoptera, Cynipoidea) 8. Cynips minuta and Xystus minutus Hartig. Entomologische Berichten 45, 1618.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics 1, 4750.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 15671587.CrossRefGoogle ScholarPubMed
Fauvergue, X., Tentelier, C., Genson, G., Audiot, P., Guillemaud, T. & Streiff, R. (2005) Microsatellite DNA markers for Lysiphlebus testaceipes. Molecular Ecology Notes 5, 109111.CrossRefGoogle Scholar
Feder, J.L., Forbes, A.A. (2010) Sequential speciation and the diversity of parasitic insects. Ecological Entomology 35, 6776.Google Scholar
Fergusson, N.D.M. (1980) A Revision of British Species of Dendrocerus Ratzeburg (Hymenoptera: Ceraphronoidea) with a Review of their Biology as Aphid Hyperparasites. London, Bulletin of the British Museum (Natural History).Google Scholar
Forbes, A.A., Powell, T.H.Q., Stelinski, L.L., Smith, J.J. & Feder, J.L. (2009) Sequential sympatric speciation across trophic levels. Science 323, 776779.CrossRefGoogle ScholarPubMed
Funk, D.J. (1998) Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52, 17441759.Google Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London Series B-Biological Sciences 263, 10031009.Google Scholar
Gaston, K.J. (1991) The magnitude of global insect species richness. Conservation Biology 5, 283296.Google Scholar
Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, Princeton University Press.Google Scholar
Goudet, J. (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes 5, 184186. Available online at http://www2.unil.ch/popgen/softwares/fstat.htm.Google Scholar
Guo, S.W. & Thompson, E.A. (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361372.Google Scholar
Jaenike, J. (1990) Host Specialization in phytophagous insects. Annual Review of Ecology and Systematics 21, 243273.Google Scholar
Kavallieratos, N.G., Tomanović, Ž., Starý, P. & Bogdanović, A.M. (2008) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Prunoideae and Maloideae crops in southeast Europe: aphidiinae–aphid–plant associations and keys. Zootaxa 1793, 4764.CrossRefGoogle Scholar
Klinkhamer, P.G.L. & de Jong, T.J. (1993) Cirsium Vulgare (Savi) Ten. Journal of Ecology 81, 177191.Google Scholar
Labandeira, C. & Sepkoski, J. (1993) Insect diversity in the fossil record. Science 261, 310315.Google Scholar
Langella, O. (1999) Populations 1.2.30. Available online at http://bioinformatics.org/~tryphon/populations/.Google Scholar
Liepert, C. (1996) Chemische Mimikry bei Blattlausparasitoiden der Gattung Lysiphlebus (Hymenoptera, Aphidiidae). PhD Thesis, Universität Bayreuth, Germany.Google Scholar
Mayhew, P.J. (2007) Why are there so many insect species? Perspectives from fossils and phylogenies. Biological Reviews 82, 425454.Google Scholar
Mitter, C., Farrell, B. & Wiegmann, B. (1988) The phylogenetic study of adaptive zones: has phytophagy promoted insect diversification? American Naturalist 132, 107128.Google Scholar
Müller, C.B., Adriaanse, I.C.T., Belshaw, R. & Godfray, H.C.J. (1999) The structure of an aphid–parasitoid community. Journal of Animal Ecology 68, 346370.Google Scholar
Nosil, P. (2007) Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. American Naturalist 169, 151162.CrossRefGoogle ScholarPubMed
Nyabuga, F.N., Loxdale, H.D., Heckel, D.G. & Weisser, W.W. (2011) Temporal genetic structuring of a specialist parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae) attacking a specialist aphid on tansy. Biological Journal of the Linnean Society 102, 737749.Google Scholar
Page, R.D.M. (1996) Tree View: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358. Available online at taxonomy.zoology.gla.ac.uk/rod/treeview.html.Google Scholar
Parks, J.C. & Werth, C.R. (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). American Journal of Botany 80, 537544.Google Scholar
Pashley, D.P. (1986) Host-associated genetic differentiation in fall armyworm (Lepidoptera: Noctuidae): a sibling species complex. Annals of the Entomological Society of America 79, 898904.Google Scholar
Pritchard, J.K., Stephens, M. & Donelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.Google Scholar
Quicke, D.L.J. (1997) Parasitic Wasps. London, Chapman and Hall.Google Scholar
Raymond, M. & Rousset, F. (1995) GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249. Available online at http://kimura.univ-montp2.fr/~rousset/Genepop.htm.Google Scholar
Rosenberg, N.A. (2004) Distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137138. Available online at http://www.stanford.edu/group/rosenberglab/distruct.html.Google Scholar
Rousset, F. (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145, 12191228.Google Scholar
Sandrock, C. & Vorburger, C. (2011) Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Current biology 21, 433437.Google Scholar
Sandrock, C., Frauenfelder, N., von Burg, S. & Vorburger, C. (2007) Microsatellite DNA markers for the aphid parasitoid Lysiphlebus fabarum and their applicability to related species. Molecular Ecology Notes 7, 10801083.Google Scholar
Sandrock, C., Gouskov, A. & Vorburger, C. (2010) Ample genetic variation but no evidence for genotype specificity in an all-parthenogenetic host–parasitoid interaction. Journal of Evolutionary Biology 23, 578585.Google Scholar
Sandrock, C., Schirrmeister, B. & Vorburger, C. (2011 a) Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evolutionary Biology 11, 348.CrossRefGoogle Scholar
Sandrock, C., Razmjou, J. & Vorburger, C. (2011 b) Climate effects on life cycle variation and population genetic architecture of the black bean aphid, Aphis fabae. Molecular Ecology 20, 41654181.Google Scholar
Schluter, D. (2001) Ecology and the origin of species. Trends in Ecology and Evolution 16, 372380.Google Scholar
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457462.Google Scholar
Smith, J.M. (1966) Sympatric speciation. American Naturalist 100, 637650.Google Scholar
Sneath, P.H.A. & Sokal, R.R. (1973) Numerical Taxonomy: The Principles and Practice of Numerical Classification. San Francisco, Freeman.Google Scholar
Starý, P. (1966) Aphid Parasitoids of Czechoslovakia: A Review of the Chechoslovak Aphidiidae, Hymenoptera. Prague, Czechoslovak Academy of Science.Google Scholar
Starý, P. (1999) Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hym., Braconidae, Aphidiinae). Journal of Applied Entomology 123, 231236.Google Scholar
Starý, P. (2006) Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae, Aphidiinae). Prague, Academia.Google Scholar
Stireman, J.O. III, Nason, J.D. & Heard, S.B. (2005) Host-associated genetic differentiation in phytophagous insects: general phenomenon or isolated exceptions? Evidence from a goldenrod-insect community. Evolution 59, 25732587.Google Scholar
Stireman, J.O. III, Nason, J.D., Heard, S.B. & Seehawer, J.M. (2006) Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proceedings of the Royal Society B: Biological Sciences 273, 523530.Google Scholar
Stork, N.E. (1988) Insect diversity: facts, fiction and speculation. Biological Journal of the Linnean Society 35, 321337.Google Scholar
Sullivan, D.J. (1987) Insect hyperparasitism. Annual Review of Entomology 32, 4970.Google Scholar
Tomanović, Ž., Kavallieratos, N.G., Starý, P., Stanisavljević, L.Ž., Ćetković, A., Stamenković, S., Jovanović, S. & Athanassiou, C.G. (2009) Regional tritrophic relationship patterns of five aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) in agroecosystem-dominated landscapes of southeastern Europe. Journal of Economic Entomology 102, 836854.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370.Google Scholar
Weisser, W.W. & Völkl, W. (1997) Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym, aphidiidae). Journal of Applied Entomology-Zeitschrift für Angewandte Entomologie 121, 2328.Google Scholar