Eur. J. Entomol. 108 (4): 635-650, 2011 | DOI: 10.14411/eje.2011.082

The parasitoid species complex associated with sexual and parthenogenetic Naryciinae (Lepidoptera: Psychidae): Integrating ecological and molecular analyses

Jelmer A. ELZINGA1, Kees ZWAKHALS2, Johanna MAPPES1, Alessandro GRAPPUTO3
1 Centre of Excellence in Evolutionary Research, Department of Biological and Environmental Science, P.O. Box 35, 40014 University of Jyväskylä, Finland; e-mails: jelmerelzinga@hotmail.com, johanna.mappes@jyu.fi
2 Dr. Dreeslaan 204, 4241 CM Arkel, The Netherlands; e-mail: keeszwakhals@yahoo.com
3 Department of Biology, University of Padua, Via Ugo Bassi 58/B, I-35121 Padua, Italy; e-mail: alessandro.grapputo@unipd.it

This study describes the parasitoid species complex associated with seven closely related species of sexual (Siederia rupicollella, S. listerella, Dahlica lazuri, D. charlottae and D. lichenella) and parthenogenetic (Dahlica fennicella and D. triquetrella) Naryciinae (Lepidoptera: Psychidae) in Central Finland. A thorough ecological analysis of all the species of parasitoids recorded was combined with analyses of molecular data. Mitochondrial and nuclear DNA data were obtained from all the species in order to (1) detect cryptic species associated with host specialization, (2) assign undescribed males to females, and (3) verify the morphological identification of closely related species. A DNA barcoding technique was employed to identify host species from parasitized larval remains. By sampling more than 10,000 host larvae, of which 25.7% were parasitized, nine parasitoid species were identified morphologically, including both koinobionts (Ichneumonidae: Diadegma incompletum, Macrus parvulus, Trachyarus borealis, T. solyanikovi, T. fuscipes, T. brevipennis and Braconidae: Meteorus affinis) and idiobionts (Ichneumonidae: Orthizema flavicorne, Gelis fuscicornis). Ecological characteristics such as time and mode of host attack, time of emergence and level of specialization differed widely. The results show that differences in parasitoid biology need to be taken into account when studying differences in percentage parasitism of sexual and parthenogenetic Naryciinae. The molecular data revealed that one parasitoid species M. parvulus may consist of two cryptic forms associated with the sexual and parthenogenetic hosts, respectively. The data further establishes that T. brevipennis and some T. fuscipes are in fact morphotypes of one species. The large variation in mitochondrial DNA within species and its inconsistency with nuclear DNA demonstrate that current species and genus delimitation is inadequate in the Trachyarus species group. Our study shows that it is essential to use DNA barcoding methods when investigating host-parasitoid complexes.

Keywords: Barcoding, larval remains, parasitism, parthenogenesis, sex ratio, COI, COII, Wingless, Hymenoptera, Braconidae, Ichneumonidae, Lepidoptera, Psychidae, Naryciinae

Received: October 1, 2010; Revised: May 5, 2011; Accepted: May 5, 2011; Published: October 3, 2011  Show citation

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ELZINGA, J.A., ZWAKHALS, K., MAPPES, J., & GRAPPUTO, A. (2011). The parasitoid species complex associated with sexual and parthenogenetic Naryciinae (Lepidoptera: Psychidae): Integrating ecological and molecular analyses. EJE108(4), 635-650. doi: 10.14411/eje.2011.082
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References

  1. AKAIKE H. 1974: A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19: 716-723 Go to original source...
  2. BARRON J.R. & BISDEE J.R. 1977: The final instars of Leptocamplex cremastoides and Macrus parvulus (Hymenoptera: Ichneumonidae: Campopleginae), and notes on the classification of the genera. Ann. Entomol. Soc. Am. 70: 290-292 Go to original source...
  3. BERNARDO U., MONTI M.M., NAPPO A.G., GEBIOLA M., RUSSO A., PEDATA P.A. & VIGGIANI G. 2008: Species status of two populations of Pnigalio soemius (Hymenoptera: Eulophidae) reared from two different hosts: an integrative approach. Biol. Contr. 46: 293-303 Go to original source...
  4. BROWER A.V.Z. & DESALLE R. 1998: Patterns of mitochondrial versus nuclear DNA sequence divergence among nymphalid butterflies: the utility of wingless as a source of characters for phylogenetic inference. Insect Mol. Biol. 7: 1-10 Go to original source...
  5. CHARNOV E.L. & SKINNER S.W. 1985: Complementary approaches to the understanding of parasitoid oviposition decisions. Environ. Entomol. 14: 383-391 Go to original source...
  6. DESNEUX N., STARY 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). Ann. Entomol. Soc. Am. 102: 925-936 Go to original source...
  7. DILLER E. 1988: Vorlaeufige Resultate einer Bearbeitung der Gattungen Hemichneumon Wesmael, 1857, und Trachyarus Thomson, 1891 (Hymenoptera, Ichneumonidae, Phaeogenini). Entomofauna 9: 369-380
  8. DORCHIN N., SCOTT E.R., CLARKIN C.E., LUONGO M.P., JORDAN S. & ABRAHAMSON W.G. 2009: Behavioural, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges. J. Evol. Biol. 22: 729-739 Go to original source...
  9. ELZINGA J.A., GRAPPUTO A., CHEVASCO V. & MAPPES J. 2011: Influence of male mating history on female reproductive success among monandrous Naryciinae (Lepidoptera: Psychidae). Ecol. Entomol. 36: 170-180 Go to original source...
  10. ELZINGA J.A., ZWAKHALS K., HARVEY J.A. & BIERE A. 2007: The parasitoid complex associated with the herbivore Hadena bicruris (Lepidoptera: Noctuidae) on Silene latifolia (Caryophyllaceae) in the Netherlands. J. Nat. Hist. 41: 101-123 Go to original source...
  11. FOLMER O., BLACK M., HOEH W., LUTZ R. & VRIJENHOEK R. 1993: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotech. 3: 294-299
  12. FORBES A.A., POWEL T.H.Q., STELINSKI L.L., SMITH J.J. & FEDER J.L. 2009: Sequential sympatric speciation across trophic levels. Science 323: 776-779 Go to original source...
  13. FREZAL L. & LEBLOIS R. 2008: Four years of DNA barcoding: Current advances and prospects. Infect. Genet. Evol. 8: 727-736 Go to original source...
  14. GODFRAY H.C.J. 1994: Parasitoids. Princeton University Press, Princeton, NJ, 488 pp
  15. GOKHMAN V. 2007: Revision of the genus Trachyarus Thomson. Spixiana 30: 65-83
  16. GRAPPUTO A., KUMPULAINEN T. & MAPPES J. 2005: Phylogeny and evolution of parthenogenesis in Finnish bagworm moth species (Lepidoptera: Psychidae: Naryciinae) based on mtDNA-markers. Ann. Zool. Fenn. 42: 141-160
  17. HAJIBABAEI M., SINGER G.A.C., HEBERT P.D.N. & HICKEY D.A. 2007: DNA barcoding: how it complements taxonomy, molecular phylogenetics and population genetics. Trends Genet. 23: 167-172 Go to original source...
  18. HEBERT P.D.N., CYWINSKA A., BALL S.L. & DEWAARD J.R. 2003: Biological identifications through DNA barcodes. Proc. R. Soc. Lond. (B, Biol. Sci.) 270: 313-321 Go to original source...
  19. HORSTMANN K. 1970: Bemerkungen zur Systematik einiger Gattungen der Campopleginae. Nachr. Bayer. Entomol. 19: 77-84
  20. HORSTMANN K. 1973: Nachtrag zur Revision der europaeischen Diadegma-arten. Beitr. Entomol. 23: 131-150
  21. KANKARE M., VAN NOUHUYS S. & HANSKI I. 2005: Genetic divergence among host-specific cryptic species in Cotesia melitaearum aggregate (Hymenoptera: Braconidae), parasitoids of checkerspot butterflies. Ann. Entomol. Soc. Am. 98: 382-394 Go to original source...
  22. KING B.H. 1987: Offspring sex ratios in parasitoid wasps. Q. Rev. Biol. 62: 367-377 Go to original source...
  23. KING K.C., DELPH L.F., JOKELA J. & LIVELY C.M. 2009: The geographic mosaic of sex and the red queen. Curr. Biol. 19: 1438-1441 Go to original source...
  24. KUMPULAINEN T., GRAPPUTO A. & MAPPES J. 2004: Parasites and sexual reproduction in psychid moths. Evolution 58: 1511-1520 Go to original source...
  25. LEPIDOPTEROLOGEN-ARBEITSGRUPPE 1997: Psychidae - Sacktraeger. In: Schmetterlinge und ihre Lebensraeume. Arten, Gefaerdung, Schutz. Schweiz und Angrenzende gebieten Band 2. Pro Natura - Schweizerische Bund fuer Naturschutz, Egg, pp. 165-308
  26. LINARES M.C., SOTO-CALDERON I.D., LEES D.C. & ANTHONY N.M. 2009: High mitochondrial diversity in geographically widespread butterflies of Madagascar: a test of the DNA barcoding approach. Mol. Phylogenet. Evol. 50: 485-495 Go to original source...
  27. MEIER R., KWONG S., VAIDYA G. & NG P.K.L. 2006: DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Syst. Biol. 55: 715-728 Go to original source...
  28. MEYER C.P. & PAULAY G. 2005: DNA barcoding: error rates based on comprehensive sampling. PLoS Biol. 3: 2229-2238 Go to original source...
  29. MITTER K.T., LARSEN T.B., DE PRINS W., DE PRINS J., COLLINS S., WEGHE G.V., SAFIAN S., ZAKHAROV E.V., HAWTHORNE D.J., KAWAHARA A.Y. & REGIER J.C. 2011: The butterfly subfamily Pseudopontiinae is not monobasic: marked genetic diversity and morphology reveal three new species of Pseudopontia (Lepidoptera: Pieridae). Syst. Entomol. 36: 139-163 Go to original source...
  30. PALMQVIST G. 2008: Psychidae, Saeckspinnare [Psychidae, Bagworm Moths]. In Bengtsson B.A. & Palmqvist G. (eds): Nationalnyckeln till Sveriges Flora och Fauna. Fjaerilar: Kaekmalar - Saeckspinnare. Lepidoptera: Micropterigidae - Psychidae. [Encyclopedia of the Swedish Flora and Fauna. Lepidoptera: Micropterigidae - Psychidae.] Swedish Species Information Centre, Swedish University of Agricultural Sciences, Uppsala, pp. 492-557 (in Swedish, English abstr.)
  31. POSADA D. 2008: jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256 Go to original source...
  32. RAMIREZ S.R., NIEH J.C., QUENTAL T.B., ROUBIK D.W., DAVID W., IMPERATRIZ-FONSECA V.L., VERA L. & PIERCE N.E. 2010: A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Mol. Phyl. Gen. 56: 519-525 Go to original source...
  33. RATNASINGHAM S. & HEBERT P.D.N. 2007: BOLD: The barcode of life data system (www.barcodinglife.org). Mol. Ecol. Notes 7: 355-364 Go to original source...
  34. RONQUIST F. & HUELSENBECK J.P. 2003: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574 Go to original source...
  35. RUBINOFF D. 2006: Utility of mitochondrial DNA barcodes in species conservation. Conserv. Biol. 20: 1026-1033 Go to original source...
  36. SCHWARZ M. & BORIANI M. 1994: Redescription of Gelis longulus (Hymenoptera: Ichneumonidae), a parasitoid of Ocnerostoma piniarellum (Lepidoptera: Yponomeutidae). Eur. J. Entomol. 91: 331-334
  37. SCHWARZ M. & SHAW M.R. 1999: Western palearctic Cryptinae (Hymenoptera: Ichneumonidae) in the National Museums of Scotland, with nomenclatural changes, taxonomic notes, rearing records and special reference to the British check list. Part 2. Genus Gelis Thunberg (Phygadeuontini: Gelina). Entomol. Gazette 50: 117-142
  38. SEEHAUSEN O. 2004: Hybridization and adaptive radiation. Trends Ecol. Evol. 19: 198-207 Go to original source...
  39. SMITH M.A., WOODLEY N.E., JANZEN D.H., HALLWACHS W. & HEBERT P.D.N. 2006: DNA barcodes reveal cryptic hostspecificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proc. Natl. Acad. Sci. USA 103: 3657-3662 Go to original source...
  40. 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. Proc. Natl. Acad. Sci. USA 104: 4967-4972 Go to original source...
  41. SONG H., BUHAY J., WHITING M. & CRANDALL K. 2008: Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc. Natl. Acad. Sci. USA 105: 13486-13491 Go to original source...
  42. TAMURA K., DUDLEY J., NEI M. & KUMAR S. 2007: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599 Go to original source...
  43. WAGENER B., REINEKE A., LOHR B. & ZEBITZ C.P.W. 2006: Phylogenetic study of Diadegma species (Hymenoptera: Ichneumonidae) inferred from analysis of mitochondrial and nuclear DNA sequences. Biol. Contr. 37: 131-140 Go to original source...
  44. YU D.S., ACHTERBERG K. VAN & HORSTMANN K. 2005: World Ichneumonidae 2004. Taxonomy, Biology, Morphology and Distribution. CD/DVD. Taxapad, Vancouver, Canada
  45. ZWAKHALS K. & ELZINGA J.A. 2009: Trachyarus borealis sp. n., a previously undescribed parasitoid of Psychidae in Finland. Mitt. Muench. Entomol. Ges. 99: 129-133

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