A molecular phylogeny of the Trichogrammatidae (Hymenoptera: Chalcidoidea), with an evaluation of the utility of their male genitalia for higher level classification

Systematic Entomology

Volumn 32, Issue 2, 2007, Pages 227-251

  Owen, Albert K ^a   George, Jeremiah ^a   Pinto, John D ^a   Heraty, John M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DATA SET; EGG PARASITOID; HOST RANGE; MOLECULAR ANALYSIS; MORPHOLOGY; PHYLOGENY; TAXONOMY; WASP;

CHALCIDOIDEA; COLEOPTERA; HEMIPTERA; HEXAPODA; HYMENOPTERA; LEPIDOPTERA; TRICHOGRAMMATIDAE;

EID: 34247373463     PISSN: 03076970     EISSN: 13653113     Source Type: Journal    
DOI: 10.1111/j.1365-3113.2006.00361.x     Document Type: Article

References (102)

1. Al-Wahaibi, A.K., Owen, A.K. & Morse, J.G. (2005) Description and behavioural biology of two Ufens species (Hymenoptera: Trichogrammatidae), egg parasitoids of Homalodisca species (Hemiptera: Cicadellidae) in southern California. Bulletin of Entomological Research, 95, 275-288.
2. Arnqvist, G. (1997) The evolution of animal genitalia: distinguishing between hypotheses by single species studies. Biological Journal of the Linnean Society, 60, 365-379.
3. Ashmead, W.H. (1904) Classification of the chalcid flies of the superfamily Chalcidoidea, with descriptions of new species in the Carnegie Museum, collected in South America by Herbert H. Smith. Memoirs of the Carnegie Museum, 1 (4).
4. Babcock, C.S. & Heraty, J.M. (2000) Molecular markers distinguishing Encarsia formosa and Encarsia luteola (Hymenoptera: Aphelinidae. Annals of the Entomological Society of America 93(4): 738-744.
5. Babcock, C.S., Heraty, J.M., De Barro, P.J., Driver, F. & Schmidt, S. (2001) Preliminary phylogeny of Encarsia Forster (Hymenoptera: Aphelinidae) based on morphology and 28S rDNA. Molecular Phylogenetics and Evolution, 18 (2), 306-323.
6. Baker, R.H. & DeSalle, R. (1997) Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Systematic Biology, 46 (4), 654-673.
7. Bakkendorf, O. (1934) Biological investigations on some Danish Hymenopterous egg-parasites, especially in Homopterous and Heteropterous eggs, with taxonomic remarks and descriptions of new species. Entomologiske Meddelelser, 19, 1-134.
8. Bao, J.-Z. & Chen, X.-H. (1989) Research and Applications of Trichogramma in China. Academic Books and Periodicals Science Press, Beijing.
9. Berbee, M.L. (1996) Loculoascomycete origins and evolution of filamentous ascomycete morphology based on 18S rRNA gene sequence data. Molecular Biology and Evolution, 13, 462-470.
10. Bergsten, J. (2005) A review of long-branch attraction. Cladistics, 21, 163-193.
11. Blood, B.N. (1923) Notes on Trichogrammatinae taken around Bristol. Proceedings of the Bristol Naturalist Society (Annual Report), 5, 253-258.
12. Boucek, Z. (1988) An overview of the higher classification of the Chalcidoidea (parasitic Hymenoptera). Advances in Parasitic Hymenoptera Research: Proceedings of the Second Conference on Taxonomy and Biology of Parasitic Hymenoptera, Gainesville, November 1987, pp. 11-23. E.J. Brill, Leiden.
13. Campbell, B., Steffen-Campbell, J. & Werren, J.H. (1993) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer ITS2 and 28S rDNA sequences. Insect Molecular Biology, 2, 225-237.
14. Campbell, B., Heraty, J.M., Rasplus, J., Chan, K., Steffen-Campbell, J. & Babcock, C. (2000) Molecular systematics of the Chalcidoidea using 28S-D2 rDNA. Hymenoptera: Evolution, Biodiversity, Biological Control (ed. by A. Austin and M. Dowton), pp. 59-73. ANIC Publishing, Melbourne.
15. Caterino, M.S., Cho, S. & Sperling, F.A.H. (2000) The current state of insect molecular systematics: a thriving tower of babel. Annual Review of Entomology, 45, 1-54.
16. Caterino,M.S., Shull, V.L., Hammond, P.M. & Vogler, A.P. (2002) Basal relationships of Coleoptera inferred from 18S rDNA sequences. Zoologica Scripta, 31 (1), 41-49.
17. Chalwatzis, N., Hauf, J., Van de Peer, Y., Kinzelbach, R. & Zimmerman, F.K. (1996) 18S ribosomal RNA genes of insects: primary structure of the genes and molecular phylogeny of the Holometabola. Annals of the Entomological Society of America, 89 (6), 788-803.
18. Delvare, G. & LaSalle, J. (2000) Trisecodes gen.n., (Hymenoptera: Eulophidae: Entedoninae), the first eulophid with three tarsal segments. Journal of Hymenoptera Research, 9 (2), 305-312.
19. Doutt, R.L. & Viggiani, G. (1968) The classification of the Trichogrammatidae (Hymenoptera: Chalcidoidea). Proceedings of the California Academy of Sciences (4th Series), 35, 477-586.
20. Dowton, M. & Austin, A. (2001) Simultaneous analysis of 16S, 28S, COI and morphology in the Hymenoptera: Aprocrita - evolutionary transitions among parasitic wasps. Biological Journal of the Linnean Society, 74, 87-111.
21. Eberhard, W.G. (1985) Sexual Selection and Animal Genitalia. Harvard University Press, Cambridge, Massachusetts.
22. George, J. (2003) A review of the Paracentrobiini (Hymenoptera: Trichogrammatidae) and a revision of the United States species of Ittys and Ittysella. MSc Thesis. Department of Entomology, University of California, Riverside, California.
23. Gerbi, S.A. (1985) Evolution of ribosomal DNA. Molecular Evolutionary Genetics (ed. by J. MacIntyre), pp. 419-517. Plenum Press, New York.
24. Gibson, G.A.P., Huber, J.T. & Woolley, J.B. (1997) Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera), 794. National Research Council Research Press, Ottawa.
25. Gibson, G.A.P., Heraty, J.M. & Woolley, J.B. (1999) Phylogenetics and classification of Chalcidoidea and Mymarommatoidea. Zoologica Scripta, 28 (1-2), 87-124.
26. Gillespie, J.J. (2004) Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules. Molecular Phylogenetics and Evolution, 33, 936-943.
27. Gillespie, J.J., Munro, J.B., Heraty, J.M., Yoder, M.J., Owen, A.K. & Carmichael, A.E. (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 for chalcidoid wasps (Hymenoptera: Chalcidoidea). Molecular Biology and Evolution, 22 (7), 1593-1608.
28. Girault, A.A. (1912) The chalcidoid family Trichogrammatidae. I. Tables of the subfamilies and genera and revised catalogue. Bulletin of Wisconsin Natural History Society, 10, 81-100.
29. Gladstein, D. & Wheeler, W. (1996) POY. Software for Direct Optimization of DNA and Other Data. American Museum of Natural History, New York.
30. Gu, X., Fu, Y.-X. & Li, W.-H. (1995) Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Molecular Biology and Evolution, 12, 546-557.
31. Gutell, R.R., Larsen, N. & Woese, C.R. (1994) Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiology Reviews, 58, 10-26.
32. Hancock, J.M., Tautz, D. et al. (1988) Evololution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster. Molecular Biology and Evolution 5 (4): 393-414.
33. Hayat, M. (1994) Notes on some genera of the Aphelinidae (Hymenoptera: Chalcidoidea), with comments on the classification of the family. Oriental Insects, 28, 81-96.
34. Heraty, J.M. (2004) Molecular systematics, Chalcidoidea and biological control. Genetics, Evolution and Biological Control (ed. by L.E. Ehler, R. Siorza and T. Mateille), pp. 39-71. CAB International, Wallingford.
35. Heraty, J.M., Hawks, D., Kostecki, J.S. & Carmichael, A. (2004) Phylogeny and behaviour of the Gollumiellinae, a new subfamily of ant-parasitic Eucharitidae (Hymenoptera: Chalcidoidea). Systematic Entomology, 29, 544-559.
36. Hosken, D.J. & Stockley, P. (2004) Sexual selection and genital evolution. Trends in Ecology and Evolution, 19 (2), 87-93.
37. Huber, J.T. & Beardsley, J.W. (2000) A new genus of fairlyfly, Kikiki, from the Hawaiian Islands (Hymenoptera: Mymaridae). Proceedings of the Hawaiian Entomological Society, 34, 65-70.
38. Huelsenbeck, J.P., Ronquist, F., Nielsen, R. & Bollback, J.P. (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294, 2310-2314.
39. Kim, J.W. (2003) Classification and evolution of the Aphelininae (Hymenoptera: Aphelinidae). PhD Thesis. Department of Entomology, University of California, Riverside, California.
40. Kim, J.W. & Triapitsyn, S.V. (2004) A new species of Pteroptrix (Hymenoptera: Aphelinidae) from Argentina, the first known aphelinid with three-segmented tarsi. Entomological News, 114 (1), 10-17.
41. Kjer, K.M. (1995) Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs. Molecular Phylogenetics and Evolution, 4 (3), 314-330.
42. Kjer, K.M. (2004) Aligned 18S and insect phylogeny. Systematic Biology, 53 (3), 506-514.
43. Kryger, J.P. (1918) The European Trichogramminae. Entomologiske Meddelelser, 12, 257-354.
44. Lanave, C., Preparata, G., Saccone, C. & Serio, G. (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution, 20 (1), 86-93.
45. Larget, B. & Simon, D. (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Molecular Biology and Evolution, 16, 750-759.
46. Lee, M.S.Y. (2001) Unalignable sequences and molecular evolution. Trends in Ecology and Evolution, 16 (12), 681-685.
47. Lin, N. (1994) Systematic Studies of Chinese Trichogrammatidae. Fuzhou, Fujian.
48. Loytynoja, A. & Milinkovitch, M.C. (2002) Proalign, a Probabilistic Multiple Alignment Program. University of Brussels, Brussels.
49. Lutzoni, F. (1997) Phylogeny of lichen- and non-lichen forming omphalinoid mushrooms and the utility of testing for compatibility among multiple data sets. Systematic Biology, 46 (3), 373-406.
50. Lutzoni, F., Wagner, P., Reeb, V. & Zoller, S. (2000) Integrating ambiguously aligned regions of DNA sequences in phylogenetic analyses without violating positional homology. Systematic Biology, 49 (4), 628-651.
51. Maddison, D. (1991) The discovery and importance of multiple islands of most parsimonious trees. Systematic Zoology, 40: 315-328.
52. Maddison, D.R. & Maddison, W.P. (2000) MacClade 4: Analysis of Phylogeny and Character Evolution, Version beta. Sinauer Associates, Inc., Sunderland, Massachusetts.
53. Mathews, D.H., Sabina, J., Zuker, M. & Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. Journal of Molecular Evolution, 288, 911-940.
54. Mercet, R.G. (1929) Notas sobre Afelínidos (Hym. Chalc.), 2a nota. EOS. Revista Española di Entomologia, 5, 111-117.
55. Miura, K. (1992) Aggressive behavior in Paracentrobia andoi (Hymenoptera, Trichogrammatidae), an egg parasitoid of the green rice leafhopper. Japanese Journal of Entomology, 60 (1), 103-107.
56. Nagaraja, H. (1978) Experimental hybridization between some species of Trichogrammatoidea Girault (Hymenoptera: Trichogrammatidae. Journal of Entomological Research 2 (2): 192-198.
57. Nagarkatti, S. and H. Nagaraja (1977) Biosystematics of Trichogramma and Trichogrammatoidea species. Annual Review of Entomology 22: 157-176.
58. Nowicki, S. (1933) Descriptions of a new genus and of new species of the superfamily Chalcidoidea (Hymenoptera). Polskie Pismo Entomologiczne, T.XXI, 1-4.
59. Noyes, J.S. (1990) A word on Chalcidoid classification. Chalcid Forum (Newsletter), 13, 6-9.
60. Noyes, J.S. (2001) Taxapad: Biological and Taxonomic Information, Chalcidoidea. The Natural History Museum, London.
61. Nunn, G.B., Theisen, B.F., Christensen, B. & Arctander, P. (1996) Simplicity-correlated size growth of the nuclear 28S ribosomal RNA D3 expansion segment in the crustacean order Isopoda. Journal of Molecular Evolution, 42, 211-223.
62. Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P. & Nieves-Aldrey, J.L. (2004) Bayesian phylogenetic analysis of combined data. Systematic Biology, 53 (1), 47-67.
63. Oatman, E.R. & Pinto, J.D. (1987) A taxonomic review of Trichogramma (Trichogrammanza) Carver (Hymenoptera: Trichogrammatidae), with descriptions of two species from Australia, Journal of the Australian Entomological Society, 26: 193-201.
64. Ouvrard, D., Campbell, B., Bourgoin, T. & Chan, K. (2000) 18S rRNA secondary structure and phylogenetic position of Peloridiidae (Insecta, Hemiptera). Molecular Phylogenetics and Evolution, 16 (3), 403-417.
65. Owen, A.K. & Pinto, J.D. (2004) Pachamama, an uncommon and distinctive new genus of Trichogrammatidae (Hymenoptera: Chalcidoidea) from tropical America. Zootaxa, 664: 1-8.
66. Page, R.D.M. (1996) TreeView: An application to display phylogenetic trees on personal computers. Computer Applications in Bioscience, 12 (4): 357-358.
67. Peck, O., Boucek, Z. & Hoffer, A. (1964) Keys to the Chalcidoidea of Czechoslovakia. Memoirs of the Entomological Society of Canada, 34, 3-112.
68. Petersen, G., Seberg, O., Aagesen, L. & Frederiksen, S. (2004) An empirical test of the treatment of indels during optimization alignment based on the phylogeny of the genus Secale (Poaceae). Molecular Phylogenetics and Evolution, 30, 733-742.
69. Pinto, J.D. (1990) The genus Xiphogramma, its occurrence in North America, and remarks on closely related genera (Hymenoptera: Trichogrammatidae. Proceedings of the Entomological Society of Washington 92: 538-543.
70. Pinto, J.D. (1997) Trichogrammatidae. Annotated Keys to the Genera of Nearctic Chalcidoidea (ed. by G.A.P. Gibson, J.T. Huber and J.B. Woolley), p. 794. NRC Research Press, Ottawa.
71. Pinto, J.D. (1999) Systematics of the North American Species of Trichogramma Westwood (Hymenoptera: Trichogrammatidae). The Entomological Society of Washington, Washington DC.
72. Pinto, J.D. (2005) Descriptions of additional new world Trichogrammatidae (Hymenoptera): the genus Nicolavespa and a new species of Haeckeliania. Proceedings of the Entomological Society of Washington, 107 (3), 627-641.
73. Pinto, J.D. (2006) A review of the New World genera of Trichogrammatidae (Hymenoptera). Journal of Hymenoptera Research, 15 (1), 38-163.
74. Pinto, J.D. & Stouthamer, R. (1994) Systematics of the Trichogrammatidae with emphasis on Trichogramma. Biological Control with Egg Parasitoids (ed. by E. Wajnberg and S.A. Hassan), pp. 1-36. CAB International, Wallingford.
75. Pinto, J.D. & George, J. (2004) Kyuwia, a new genus of Trichogrammatidae (Hymenoptera) from Africa. Proceedings of the Entomological Society of Washington, 106 (3): 531-539.
76. Pinto, J.D. & Owen, A.K. (2004) Adryas, a new genus of Trichogrammatidae (Hymenoptera: Chalcidoidea) from the New World tropics. Proceedings of the Entomological Society of Washington, 106 (4): 905-922.
77. Pinto, J.D. & Viggiani, G. (1988) Two new Trichogrammatidae (Hymenoptera) from North America: Ittysella lagunera Pinto and Viggiani (N.Gen., N.Sp.) and Epoligosita mexicana Viggiani (N.Sp.). Pan-Pacific Entomologist, 63 (4): 371-376.
78. Pinto, J.D. & Viggiani, G. (1991) A taxonomic study of the genus Ceratogramma (Hymenoptera: Trichogrammatidae). Proceedings of the Entomological Society of Washington, 93 (3): 719-732.
79. Pinto, J.D. & Viggiani, G. (2004) A review of the genera of Oligositini (Hymenoptera: Trichogrammatidae) with a preliminary hypothesis of phylogenetic relationships. Journal of Hymenoptera Research, 13 (2), 269-294.
80. Pintureau, B., del Iglesias Calvin, M. & Grenier, S. (1997) Effectiveness of the second mating in a bisexual Trichogramma species and the first mating in a thelytokous Trichogramma species (Hymenoptera: Trichogrammatidae). Canadian Entomologist, 129, 35-41.
81. Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14 (9), 817-818.
82. Rasplus, J.Y., Kerdelhue, C. & Mondor, G. (1998) Molecular phylogeny of fig wasps: Agaonidae are not monophyletic. Compte Rendu de l'Academie des Sciences de Paris, 321, 517-521.
83. Schulmeister, S. (2003) Simultaneous analysis of basal Hymenoptera (Insecta): introducing robust-choice sensitivity analysis. Biological Journal of the Linnean Society, 79, 245-275.
84. Shafee, S.A. & Rizvi, S. (1990) Classification and phylogeny of the family Aphelinidae (Hymenoptera: Chalcidoidea). Indian Journal of Systematic Entomology, 7, 103-115.
85. Shimodaira, H. & Hasegawa, M. (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution, 16, 1114-1116.
86. Sirot, L.K. (2003) The evolution of insect mating structures through sexual selection. Florida Entomologist, 86 (2), 124-133.
87. Sorenson, M.D. (1999) TreeRot, Version 2c. Boston University, Boston, Massachusetts.
88. Sorenson, J.T., Campbell, B.C., Gill, R.J. & Steffen-Campbell, J.D. (1995) Non-monophyly of Auchenorryncha ('Homoptera'), based upon 18S rDNA phylogeny: eco-evolutionary and cladistic implications within pre-Heteropterodea Hemiptera (S.L.) and a proposal for a new monophyletic suborder. Pan-Pacific Entomologist, 71, 31-60.
89. Swofford, D.L. (2001) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, Massachusetts.
90. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24, 4876-4882.
91. Velten, R.K. & Pinto, J.D. (1990) Soikiella Nowicki (Hymenoptera: Trichogrammatidae): Occurrence in North America, description of a new species, and association of the male. Pan-Pacific Entomologist, 66 (3), 246-250.
92. Viggiani, G. (1971) Ricerche sugli Hymenoptera Chalcidoidea XXVIII. Studio morfologico comparativo dell'armatura genitale esterne maschile dei Trichogrammatidae. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri' di Portici, 29, 181-222.
93. Viggiani, G. (1984) Further contribution to the knowledge of the male genitalia in the Trichogrammatidae (Hym. Chalcidoidea). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri' di Portici, 41, 173-182.
94. Viggiani, G. (1985) A new species of Zagella (Hym. Trichogrammatidae) from Florida. Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri' di Portici, 42, 15-17.
95. Viggiani, G. (1988) Description of Pintoa nearctica gen. nov., sp. nov. (Hymenoptera: Trichogrammatidae). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri' di Portici, 45, 23-29.
96. Viggiani, G. & Battaglia, D. (1984) Male genitalia in the Aphelinidae (Hym. Chalcidoidea). Bollettino del Laboratorio di Entomologia Agraria 'Filippo Silvestri' di Portici, 41, 149-172.
97. Walsh, R.S., Metzer, D.A. & Higuchi, R. (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques, 10, 506-513.
98. Wheeler, W.C., Whiting, M., Wheeler, Q.D. & Carpenter, J.M. (2001) The phylogeny of the extant hexapod orders. Cladistics, 17, 113-169.
99. Whiting, M. (2002) Phylogeny of the holometabolous insect orders: molecular evidence. Zoologica Scripta, 31, 3-15.
100. Whiting, M., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1-68.
101. Yang, Z. (1994) Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution, 39, 306-314.
102. Yousuf, M. & Shafee, S.A. (1987) Taxonomy of Indian Trichogrammatidae (Hymenoptera: Chalcidoidea). Indian Journal of Systematic Entomology, 4 (2), 55-200.