Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-14T04:42:01.095Z Has data issue: false hasContentIssue false
  • English
  • Français

Testing species limits of Eurytomidae (Hymenoptera) associated with galls induced by Diplolepis (Hymenoptera: Cynipidae) in Canada using an integrative approach

Published online by Cambridge University Press:  21 November 2013

Y. Miles Zhang ,
Michael W. Gates  and
Joseph D. Shorthouse
Y. Miles Zhang*
Affiliation:
Department of Biology, Laurentian University, Sudbury, Ontario, Canada P3E 2C6
Michael W. Gates
Affiliation:
United States Department of Agriculture, Systematic Entomology Laboratory, Agriculture Research Service, c/o National Museum of Natural History, Washington, DC 20013-7012, United States of America
Joseph D. Shorthouse
Affiliation:
Department of Biology, Laurentian University, Sudbury, Ontario, Canada P3E 2C6
*
1Corresponding author (e-mail: yuanmeng.zhang@gmail.com).
Get access Rights & Permissions [Opens in a new window]

Abstract

Studies of insect host-parasitoid relationships are often confounded by the difficulties associated with species delimitation in taxonomically challenging groups. Eurytomidae (Hymenoptera) are common parasitoids associated with galls induced by Cynipidae (Hymenoptera) and are difficult to identify due to their small size, morphological conservatism, and unreliable published host records. This study tests the species limits of eurytomids associated with galls induced by Diplolepis Geoffroy (Hymenoptera: Cynipidae) in Canada using an integrative taxonomy approach including adult morphology, the mitochondrial gene cytochrome c oxidase I, host records, and geographical range. Incongruences between morphological and molecular data were found within the Eurytoma discordans Bugbee complex, as Eurytoma discordans, Eurytoma acuta Bugbee, and Eurytoma calcarea Bugbee were shown to be new synonyms. The results also revealed the presence of cryptic species within Eurytoma spongiosa Bugbee. Furthermore, issues that have impeded ecological and biological studies of eurytomids associated with rose galls such as host specificity and sex association were resolved using DNA barcodes, providing new insights into the evolutionary history of this difficult group.

Résumé

Les études sur les interactions hôtes-parasitoïdes chez les insectes sont souvent limitées par les difficultés associées à l'identification des espèces, surtout lorsqu'elles proviennent de groupes taxonomiques complexes. Les Eurytomidae (Hymenoptera) sont des parasitoïdes communs associés aux galles formées par les Cynipidae (Hymenoptera), et leur identification peut s'avérer laborieuse en raison de leur taille minuscule, leur similitude morphologique et un recueil peu fiable des espèces d'hôtes connues. Le but de cette étude est de redéfinir les limites taxonomiques des eurytomides associés aux galles formées par Diplolepis Geoffroy (Hymenoptera: Cynipidae) au Canada en utilisant une méthodologie taxonomique intégrée basée sur la morphologie des adultes, le gène mitochondrial cytochrome c oxidase I, les hôtes exploités et l’étendue géographique des espèces. Nous avons noté certaines incompatibilités entre les données morphologiques et moléculaires dans le complexe de Eurytoma discordans Bugbee, trois espèces s'avérant analogues. Nos résultats révèlent également la présence d'espèces cryptiques au sein d’Eurytoma spongiosa Bugbee. Cette étude démontre donc que les difficultés rencontrées lors de recherches écologiques et biologiques sur les eurytomides associés aux galles des rosiers, comme par exemple leur spécifité d'hôtes et l'identification des sexes, peuvent être contournées par l'utilisation de marqueurs génétiques. Cette méthodologie permettra ainsi d'approfondir nos connaissances de l'histoire évolutive de ce groupe taxonomique complexe.

Type
Biodiversity & Evolution
Information
The Canadian Entomologist , Volume 146 , Issue 3 , June 2014 , pp. 321 - 334
Copyright
Copyright © Entomological Society of Canada 2013 

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.)

Footnotes

Subject editor: Patrice Bouchard

References

Ács, Z., Challis, R., Bihari, P., Blaxter, M., Hayward, A., Melika, G., et al. 2010. Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the western Palearctic. Molecular Phylogenetics and Evolution, 55: 210–225.CrossRefGoogle Scholar
Ács, Z., Melika, G., Kalo, P., Kiss, G.B. 2002. Molecular analysis in Eurytoma rosae species-group (Chalcidoidea: Eurytomidae). In Parasitic wasps: evolution, systematics, biodiversity and biological control . Edited by G. Melika and C. Thuróczy. Agroinform, Budapest, Hungary. Pp. 234–240.Google Scholar
Bordenstein, S.R., O'Hara, F.P., Werren, J.H. 2001. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature, 409: 707–710.CrossRefGoogle ScholarPubMed
Brooks, S.E.Shorthouse, J.D. 1997. Biology of the rose stem galler Diplolepis nodulosa (Hymenoptera: Cynipidae) and its associated component community in central Ontario. The Canadian Entomologist, 129: 1121–1140.CrossRefGoogle Scholar
Bugbee, R.E. 1951a. A new genus of two previously described and two new species of the Family Eurytomidae bred from cynipid and dipterous hosts. Journal of the Kansas Entomological Society, 24: 37–45.Google Scholar
Bugbee, R.E. 1951b. New and described parasites of the genus Eurytoma Illiger from rose galls caused by species of the cynipid genus Diplolepis Geoffrey. Annals of the Entomological Society of America, 44: 213–261.CrossRefGoogle Scholar
Bugbee, R.E. 1967. Revision of chalcid wasps of genus Eurytoma in America north of Mexico. Proceedings of the United States National Museum, 118: 433–552.CrossRefGoogle Scholar
Bugbee, R.E. 1973. New species of the genus Eurytoma from the United States and Canada (Hymenoptera: Eurytomidae). Journal of the Georgia Entomological Society, 8: 11–15.Google Scholar
Claridge, M.F.Askew, R.R. 1960. Sibling species in the Eurytoma rosae group (Hym: Eurytomidae). Entomophaga, 5: 141–153.CrossRefGoogle Scholar
Cognato, A.I. 2006. Standard percent DNA sequence difference for insects does not predict species boundaries. Journal of Economic Entomology, 99: 1037–1045.CrossRefGoogle Scholar
Csóka, G., Stone, G.N., Melika, G. 2005. Biology, ecology and evolution of gall-inducing Cynipidae. In Biology, ecology, and evolution of gall-inducing arthropods, volume 2 . Edited by A, Raman, C.W. Schaefer, and T.M. Withers. Science Publishers, Enfield, New Hampshire, United States of America. Pp. 573–642.Google Scholar
Dayrat, B. 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society, 85: 407–415.CrossRefGoogle Scholar
Dowton, M.Austin, A.D. 1995. Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. Journal of Molecular Evolution, 41: 958–965.CrossRefGoogle ScholarPubMed
Gates, M. 2008. Species revision and generic systematics of world Rileyinae. Vol. 127. University of California Press Publications in Entomology, Berkeley, California, United States of America. 332 pp.Google Scholar
Gates, M.W.Pérez-Lachaud, G. 2012. Description of Camponotophilus delvarei, gen. n. and sp. n. (Hymenoptera: Chalcidoidea: Eurytomidae), with discussion of diagnostic characters. Proceedings of the Entomological Society of Washington, 114: 111–124.CrossRefGoogle Scholar
Gebiola, M., Goméz-Zurita, J., Monti, M.M., Navones, P., Bernardo, U. 2012. Integration of molecular, ecological, morphological and endosymbiont data for species delimitation within the Pnigalio soemius complex (Hymenoptera: Eulophidae). Molecular Ecology, 21: 1190–2108.CrossRefGoogle ScholarPubMed
Gibson, G.A.P., Heraty, J.M., Woolley, J.B. 1999. Phylogenetics and classification of Chalcidoidea and Mymarommatoidea – a review of current concepts (Hymenoptera, Apocrita). Zoologica Scripta, 28: 87–124.CrossRefGoogle Scholar
Gibson, G.A.P., Huber, J.T., Woolley, J.B. 1997. Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). National Research Council Research Press, Ottawa, Ontario, Canada.Google Scholar
Gómez, J.F., Nieves-Aldrey, J.L., Hernández Nieves, M., Stone, G.N. 2011. Comparative morphology and biology of terminal-instar larvae of some Eurytoma (Hym. Eurytomidae) species parasitoids of gall wasps (Hym. Cynipidae) in western-Europe. Zoosystema, 33: 287–323.CrossRefGoogle Scholar
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H., Hallwachs, W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America, 101: 14812–14817.CrossRefGoogle ScholarPubMed
Henneicke, K., Dawah, H.A., Jervis, M.A. 1992. Taxonomy and biology of the final-instar larvae of some Eurytomidae (Hymenoptera: Chalcidoidea) associated with grasses in the UK. Journal of Natural History, 26: 1047–1087.CrossRefGoogle Scholar
Heraty, J. 2009. Parasitoid biodiversity and insect pest management. In Insect biodiversity: science and society . Edited by R.G. Foottit and P.H. Adler. Wiley-Blackwell, Chichester, United Kingdom. Pp. 445–462.CrossRefGoogle Scholar
Heraty, J.Hawks, D. 1998. Hexamethyldisilazane – a chemical alternative for drying insects. Entomological News, 109: 369–374.Google Scholar
Ivanova, N.V., deWaard, J.R., Hebert, P.D.N. 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6: 998–1002.CrossRefGoogle Scholar
Ivanova, N.V., deWaard, J.R., Hebert, P.D.N. 2007. CCDB protocols, glass fiber plate DNA extraction [online]. Available from http://www.dnabarcoding.ca/CCDB_DOCS/CCDB_DNA_Extraction.pdf [accessed 15 April 2012].Google Scholar
Ivanova, N.V.Grainger, C.M. 2007a. CCDB protocols, COI amplification [online]. Available from http://www.dnabarcoding.ca/CCDB_DOCS/CCDB_Amplification.pdf [accessed 15 April 2012].Google Scholar
Ivanova, N.V.Grainger, C.M. 2007b. CCDB protocols, sequencing. Available from http://www.dnabarcoding.ca/CCDB_DOCS/CCDB_Sequencing.pdf [accessed 15 April 2012].Google Scholar
Kaartinen, R., Stone, G.N., Hearn, J., Lohse, K., Roslin, T. 2010. Revealing secret liaisons: DNA barcoding changes our understanding of food webs. Ecological Entomology, 35: 623–638.CrossRefGoogle Scholar
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16: 111–120.CrossRefGoogle ScholarPubMed
Leggo, J.J.Shorthouse, J.D. 2006. Modification of galls of Diplolepis triforma (Hymenoptera: Cynipidae) by the parasitoids Eurytoma spongiosa (Hymenoptera: Eurytomidae) and Glyphomerus stigma (Hymenoptera: Torymidae). The Canadian Entomologist, 138: 681–696.CrossRefGoogle Scholar
Li, Y.W., Zhou, X., Feng, G., Hu, H., Niu, L., Hebert, P.D.N., et al. 2010. COI and ITS2 sequences delimit species, reveal cryptic taxa and host specificity of fig-associated Sycophila (Hymenoptera, Eurytomidae). Molecular Ecology Resources, 10: 31–40.CrossRefGoogle ScholarPubMed
Lotfalizadeh, H., Delvare, G., Rasplus, J.-Y. 2007a. Eurytoma caninae sp. n. (Hymenoptera, Eurytomidae), a common species previously overlooked with E. rosae. Zootaxa, 1640: 55–68.CrossRefGoogle Scholar
Lotfalizadeh, H., Delvare, G., Rasplus, J.-Y. 2007b. Phylogenetic analysis of Eurytominae (Chalcidoidea: Eurytomidae) based on morphological characters. Zoological Journal of the Linnean Society, 151: 441–510.CrossRefGoogle Scholar
Lunt, D., Zhang, D.-X., Szymura, J., Hewitt, G.M. 1996. The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Molecular Biology, 5: 153–165.CrossRefGoogle ScholarPubMed
Meier, R., Shiyang, K., Vaidya, G., Ng, P. 2006. DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology, 55: 715–728.CrossRefGoogle ScholarPubMed
Munro, J.B., Heraty, J.M., Burks, R.A., Hawks, D., Mottern, J., Cruaud, A., et al. 2011. A molecular phylogeny of the Chalcidoidea (Hymenoptera). Public Library of Science One, 6: e27023.Google ScholarPubMed
Nicholls, J.A., Preuss, S., Hayward, A., Melika, G., Csóka, G., Nieves-Aldrey, J.-L., et al. 2010. Concordant phylogeography and cryptic speciation in two western Palearctic oak gall parasitoid species complexes. Molecular Ecology, 19: 592–609.CrossRefGoogle Scholar
Noyes, J.S. 2012. Universal Chalcidoidea database [online]. Available from http://www.nhm.ac.uk/chalcidoids/ [accessed 28 April 2012].Google Scholar
Oliveira, D.C.S.G., Raychoudhury, R., Lavrov, D.V., Werren, J.H. 2008. Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Molecular Biology and Evolution, 25: 2167–2180.CrossRefGoogle ScholarPubMed
Plantard, O., Rasplus, J.-Y., Hochberg, M.E. 1996. Resource partitioning in the parasitoid assemblage of the oak galler Neuroterus quercusbaccarum L. (Hymenoptera: Cynipidae). Acta Oecologica, 17: 1–15.Google Scholar
Plantard, O., Rasplus, J.-Y., Mondor, G., Le Clainche, I., Solignac, M. 1999. Distribution and phylogeny of Wolbachia-inducing thelytoky in Rhoditini and ‘Aylacini’ (Hymenoptera: Cynipidae). Insect Molecular Biology, 8: 185–191.Google ScholarPubMed
Plantard, O., Shorthouse, J.D., Rasplus, J.-Y. 1998. Molecular phylogeny of the genus Diplolepis (Hymenoptera: Cynipidae). In The biology of gall-inducing arthropods. United States Forest Service General Technical Report NC-199 . Edited by G. Csóka, W.J. Mattson, G.N. Stone, and P.W. Price. United States Department of Agriculture, Washington, DC, United States of America. Pp. 247–260.Google Scholar
Porco, D., Rougerie, R., Deharveng, L., Hebert, P. 2010. Coupling non-destructive DNA extraction and voucher retrieval for small soft-bodied Arthropods in a high-throughput context: the example of Collembola. Molecular Ecology Resources, 10: 942–945.CrossRefGoogle Scholar
Posada, D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25: 1253–1256.CrossRefGoogle ScholarPubMed
Price, P.W., Fernandes, G.W., Waring, G.L. 1987. Adaptive nature of insect galls. Environmental Entomology, 16: 15–24.CrossRefGoogle Scholar
Ratnasingham, S.Hebert, P.D.N. 2007. BOLD: the barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes, 7: 183–189.Google Scholar
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61: 539–542.CrossRefGoogle ScholarPubMed
Santos, A.M.C., Besnard, G., Quicke, D.J. 2011. Applying DNA barcoding for the study of geographical variation in host-parasitoid interactions. Molecular Ecology Resources, 11: 46–59.CrossRefGoogle Scholar
Schönrogge, K., Stone, G.N., Crawley, M.J. 1995. Spatial and temporal variation in guild structure: parasitoids and inquilines of Andricus quercuscalicis (Hymenoptera: Cynipidae) in its native and alien ranges. Oikos, 72: 51–60.CrossRefGoogle Scholar
Schönrogge, K., Stone, G.N., Crawley, M.J. 1996. Abundance patterns and species richness of the parasitoids and inquilines of the alien gall former Andricus quercuscalicis Burgsdorf (Hymenoptera: Cynipidae). Oikos, 77: 507–518.CrossRefGoogle Scholar
Sheffield, C.S., Hebert, P.D.N., Kevan, P.G., Packer, L. 2009. DNA barcoding a regional bee (Hymenoptera: Apoidea) fauna and its potential for ecological studies. Molecular Ecology Resources, 9: 196–207.CrossRefGoogle ScholarPubMed
Shorthouse, D.P. 2012. SimpleMappr, an online tool to produce publication-quality point maps [online]. Available from www.simplemappr.net [accessed 3 April 2012].Google Scholar
Shorthouse, J.D. 1973. The insect community associated with rose galls of Diplolepis polita (Cynipidae, Hymenoptera). Quaestiones Entomologicae, 9: 55–98.Google Scholar
Shorthouse, J.D. 1988. Occurrence of two gall wasps of the genus Diplolepis (Hymenoptera: Cynipidae) on the domestic shrub rose, Rosa rugosa Thunb. (Rosaceae). The Canadian Entomologist, 120: 727–737.CrossRefGoogle Scholar
Shorthouse, J.D. 2010. Galls induced by cynipid wasps of the genus Diplolepis (Hymenoptera: Cynipidae) on the roses of Canada's grasslands. In Arthropods of Canadian grasslands (volume 1): ecology and interactions in grassland habitats . Edited by J.D. Shorthouse and K.D. Floate. Biological Survey of Canada, Ottawa, Ontario, Canada. Pp. 251–279.CrossRefGoogle Scholar
Shorthouse, J.D., Leggo, J.J., Sliva, M.D., Lalonde, R.G. 2005. Has egg location influenced the radiation of Diplolepis (Hymenoptera: Cynipidae) gall wasps on wild roses? Basic and Applied Ecology, 6: 423–434.CrossRefGoogle 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. Annals of the Entomological Society of America, 87: 651–701.CrossRefGoogle Scholar
Smith, M.A., Bertrand, C., Crosby, K., Eveleigh, E.S., Fernandez-Triana, J., Fisher, B.L., et al. 2012. Wolbachia and DNA barcoding insects: patterns, potential, and problems. Public Library of Science One, 7: e36514.Google ScholarPubMed
Smith, M.A., Fisher, B.L., Hebert, P.D.N. 2005. DNA barcoding for effective biodiversity assessment of a hyperdiverse arthropod group: the ants of Madagascar. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 360: 1825–1834.CrossRefGoogle Scholar
Smith, M.A., Rodriguez, J.J., Whitfield, J.B., Deans, A.R., Janzen, D.H., Hallwachs, W., et al. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America, 105: 12359–12364.CrossRefGoogle ScholarPubMed
Smith, M.A., Wood, D.M., Janzen, D.H., Hallwachs, W., Hebert, P.D.N. 2007. DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences of the United States of America, 104: 4967–4972.CrossRefGoogle Scholar
Smith, M.A., Woodley, N.E., Janzen, D.H., Hallwachs, W., Hebert, P.D.N. 2006. DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America, 103: 3657–3662.CrossRefGoogle ScholarPubMed
Stille, B. 1984. The effect of host plant and parasitoids on the reproductive success of the parthenogenetic gallwasp Diplolepis rosae (Hymenoptera; Cynipidae). Oecologia, 63: 364–369.CrossRefGoogle Scholar
Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D., Pujade-Villar, J. 2002. The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633–668.CrossRefGoogle ScholarPubMed
Sun, X.-J., Xiao, J.-H., Cook, J.M., Feng, G., Huang, D.-W. 2011. Comparison of host mitochondrial, nuclear and endosymbiont bacterial genes reveal cryptic fig wasp species and the effects of Wolbachia on host mtDNA evolution and diversity. BMC Evolutionary Biology, 11: 86.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular biology and evolution, 28: 2731–2739.CrossRefGoogle ScholarPubMed
Werren, J.H., Baldo, L., Clark, M.E. 2008. Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6: 741–751.CrossRefGoogle ScholarPubMed
Will, K.G., Mishler, B.D., Wheeler, Q.D. 2005. The perils of DNA barcoding and the need for integrative taxonomy. Systematic Biology, 54: 844–851.CrossRefGoogle ScholarPubMed
Xiao, J.H., Jia, J.G., Murphy, R.W., Huang, D.W. 2011. Rapid evolution of the mitochondrial genome in chalcidoid wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. Public Library of Science One, 6: e26645.Google ScholarPubMed