Systematics of the cyclostome subfamilies of braconid parasitic wasps (Hymenoptera: Ichneumonoidea): A simultaneous molecular and morphological Bayesian approach

Molecular Phylogenetics and Evolution

Volumn 38, Issue 1, 2006, Pages 130-145

  Zaldivar Riverón, Alejandro ^a,b,c   Mori, Miharu ^a,b   Quicke, Donald L J ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Ambiguously aligned regions; Braconidae; Fragment level alignment; Phylogeny; Simultaneous analysis

Indexed keywords

RNA 28S;

ANIMAL; ARTICLE; BAYES THEOREM; CLASSIFICATION; GENETICS; HISTOLOGY; PHYLOGENY; WASP;

ANIMALS; BAYES THEOREM; PHYLOGENY; RNA, RIBOSOMAL, 28S; WASPS;

BRACONIDAE; HYMENOPTERA; ICHNEUMONOIDEA; VESPOIDEA;

EID: 28844491865     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2005.08.006     Document Type: Article

References (91)

1. C. van Achterberg Essay of the phylogeny of Braconidae (Hymenoptera: Ichneumonoidea) Entomol. Tidskr. 105 1984 41 58
2. C. van Achterberg Revision of the genera of the afrotropical and w. palearctic rogadinae foerster (Hymenoptera: Braconidae) Zool. Verh. Leiden 273 1991 1 102
3. C. van Achterberg Generic revision of the subfamily Betylobraconinae (Hymenoptera: Braconidae) and other groups with modified fore tarsus Zool. Verh. Leiden 298 1995 1 342
4. C. van Achterberg, and D.L.J. Quicke Phylogeny of the subfamilies of the family braconidae: A reassessment assessed Cladistics 8 1992 237 264
5. R.R. Askew, and M.R. Shaw Parasitoid communities: their size, structure, and development J. Waage G. Greathead Insect Parasitoids 1986 Academic Press London 225 264
6. A.D. Austin, and P.C. Dangerfield A new species of Jarra Marsh and Austin (Hymenoptera: Braconidae) with comments on other parasitoids associated with the eucalypt longicorn Phoracantha semipunctata (F.) (Coleoptera: Cerambycidae) Austr. J. Entomol. 36 1997 327 331
7. A.D. Austin, and P.C. Dangerfield Biology of Mesostoa kerri (Insecta: Hymenoptera: Braconidae: Mesostoinae), an endemic Australian wasp that causes stem galls on Banskia marginata Austr. J. Bot. 46 1998 559 569
8. S.A. Belokobylskij On the division of the tribe Exothecini s.l. (Hymenoptera, Braconidae) in two with description of the new genus and subgenus Zool. Zhurn. 63 1984 1019 1026 (in Russian)
9. S.A. Belokobilskij, A. Zaldivar-Riverón, and D.L.J. Quicke Phylogeny of the genera of the parasitic wasps subfamily Doryctinae (Hymenoptera: Braconidae) based on morphological evidence Zool. J. Linn. Soc. 142 2004 369 404
10. R. Belshaw, and D.L.J. Quicke A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae) Mol. Phylogenet. Evol. 7 1997 281 293
11. R. Belshaw, and D.L.J. Quicke Robustness of ancestral state estimates: evolution of life History strategy in ichneumonoid parasitoids Syst. Biol. 51 2002 450 477
12. R. Belshaw, A. Grafen, and D.L.J. Quicke Inferring life history ovipositor morphology in parasitoid wasps using phylogenetic regression and discriminant analysis Zool. J. Linn. Soc. 139 2003 213 228
13. R. Belshaw, M. Dowton, D.L.J. Quicke, and A.D. Austin Estimating ancestral geographic distributions: a Gondwanan origin for aphid parasitoids Proc. R. Soc. Series B 267 2000 491 496
14. R. Belshaw, E. Herniou, C. Gimeno, M.G. Fitton, and D.L.J. Quicke Molecular phylogeny of the Ichneumonoidea (Hymenoptera) based on D2 expansion region of 28S rDNA Syst. Entomol. 23 1998 109 123
15. A.V.Z. Brower, and V. Schawaroch Three steps of homology assessment Cladistics 12 1996 265 272
16. M. Capek A new classification of the Braconidae (Hymenoptera) based on the cephalic structures of the final instar larva and biological evidence Can. Entomol. 102 1970 846 875
17. X. Chen, M. Piao, J.B. Whitfield, and J.H. He A molecular phylogeny of the subfamily Rogadinae (Hymenoptera: Braconidae) based on the D2 variable region of 28S ribosomal RNA Acta Entomol. Sin. 46 2003 209 217
18. C.W. Cunningham Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an iterative procedure of choosing among phylogenetic methods Syst. Biol. 46 1997 464 478
19. B.N. Danforth, L. Conway, and S. Ji Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively clade of bees (Hymenoptera: Halictidae) Syst. Biol. 52 2003 23 36
20. K. Dolphin, and D.L.J. Quicke Estimating the global species richness of an incompletely described taxon: an example using parasitoid wasps Biol. J. Linn. Soc. 73 2001 279 286
21. M. Dowton Relationships among the cyclostome braconid (Hymenoptera: Braconidae) subfamilies inferred from a mitochondrial tRNA rearrangement Mol. Phylogenet. Evol. 11 1999 283 287
22. M. Dowton, and A.D. Austin Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera J. Mol. Evol. 41 1995 958 965
23. M. Dowton, and A.D. Austin Evidence for AT-T transversion bias in wasp (Hymenoptera: Symphyta) J. Mol. Evol. 44 1997 398 405
24. M. Dowton, A.D. Austin, and M.F. Antolin Evolutionary relationships among the Braconidae (Hymenoptera: Ichneumonidea) inferred from partial 16rDNA gene sequences Insect Mol. Biol. 7 1998 129 150
25. M. Dowton, R. Belshaw, A.D. Austin, and D.L.J. Quicke Simultaneous molecular and morphological analysis of braconid relationships (Insecta: Hymenoptera: Braconidae) indicates independent mt-tRNA gene inversions within a single wasp family J. Mol. Evol. 54 2002 210 226
26. K.M. Edson, and S.B. Vinson A comparative morphology of the venom apparatus of female braconids (Hymenoptera: Braconidae) Can Entomol. 111 1979 1013 1024
27. J.S. Farris, M. Käjersjö, A.G. Kluge, and C. Bult Constructing a significance test for incongruence Cladistics 10 1994 315 319
28. Flores, S., Nassar, J.M., Quicke, D.L.J. Reproductive phenology and predispersal predation in Protium tovarense (Burseraceae), with description of the first known phytophagous Bracon species (Hymenoptera: Braconidae: Braconinae). J. Nat. Hist., in press.
29. O. Folmer, M. Black, W. Hoeh, R. Lutz, and R. Vrijenhoek DNA primers for amplification of mithochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates Mol. Mar. Biol. Biotechnol. 3 1994 294 299
30. J.J. Gillespie Characterizing regions of ambiguous alignment caused by the expansion and contraction of hairpin-stem loops in ribosomal RNA molecules Mol. Phylogenet. Evol. 33 2004 936 943
31. Gladstein, D., Wheeler, W., 1996. POY: Software for direct optimisation of DNA and other data, American Museum of Natural History (ftp://ftp.amnh.org/ pub/molecular/poy ).
32. H.C.J. Godfray Parasitoids: behavioural and evolutionary ecology 1993 Princeton Univ. Press Princeton, NJ
33. A. Graybeal Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47 1998 9 17
34. D.M. Hillis Inferring complex phylogenies Nature 383 1996 130 131
35. D.M. Hillis Taxonomic sampling, phylogenetic accuracy, and investigator bias Syst. Biol. 47 1998 3 8
36. D.M. Hillis, and J.J. Bull An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis Syst. Biol. 42 1993 182 192
37. F. Infante, P. Hanson, and R. Wharton Phytophagy in the genus Monitoriella (Hymenoptera: Braconidae) with description of new species Ann. Entomol. Soc. Am. 88 1995 406 415
38. K.M. Kjer Use of rRNA secondary structure in phylogenetic studies to identify homologous positions: an example of alignment and data presentation from the frogs Mol. Phylogenet. Evol. 4 1995 314 330
39. K.M. Kjer, R.J. Blahnik, and R.W. Holzenthal Phylogeny of Trichoptera (Caddifishes): characterization of signal and noise within multiple data sets Syst. Biol. 50 2001 781 816
40. C.G. Lanave, C. Preparata, C. Saccone, and G. Serio A new method for calculating evolutionary substitution rates J. Mol. Evol. 20 1984 86 93
41. M.S.Y. Lee Uninformative characters and apparent conflict between molecules and morphology Mol. Biol. Evol. 18 2001 676 680
42. M.S.Y. Lee Unalignable sequences and molecular evolution Trends Ecol. Evol. 16 2001 681 685
43. P.O. Lewis A likelihood approach to estimating phylogeny from discrete morphological character data Syst. Biol. 50 2001 913 925
44. C.P. Lin, and B.N. Danforth How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined data sets Mol. Phylogenet. Evol. 30 2004 686 702
45. F. Lutzoni, P. Wagner, V. Reeb, and S. Zoller Integrating ambiguously aligned regions of DNA sequences in phylogenetic analysis without violating positional homology Syst. Biol. 4 2000 628 651
46. P. Mardulyn, and J.B. Whitfield Phylogenetic signal in the COI, 16S, and 28S genes for inferring relationships among genera of Micrograstrinae (Hymenoptera; Braconidae): evidence of a high diversification rate in this group of parasitoids Mol. Phylogenet. Evol. 12 1999 282 294
47. P.M. Marsh The Doryctinae of Costa Rica (excluding the genus Heterospilus) Mem. Am. Entomol. Inst. 70 2002 1 319
48. O. Niehuis, and J.H. Wägele Phylogenetic analysis of the mitochondrial genes LSU rRNA and COI suggests early adaptive differentiation of anal teeth in chrysidine cuckoo wasps (Hymenoptera: Chrysididae) Mol. Phylogenet. Evol. 30 2004 615 622
49. D.D. Pollock, D.J. Zwickl, J.A. McGuire, and D.M. Hillis Increased taxon sampling is advantageous for phylogenetic inference Syst. Biol. 51 2002 664 671
50. D. Posada, and K.A. Crandall MODELTEST: testing the model of DNA substitution Bioinformatics 14 1998 817 818
51. D.L.J. Quicke The polyphyletic origin of endoparasitism in the cyclostome lineages of Braconidae (Hymenoptera): a reassessment Zool. Med. Leiden 67 1993 159 177
52. D.L.J. Quicke First record of Leptorhaconotus Granger (Hymenoptera: Braconidae) from South Africa, with the description of a remarkable new species and a discussion of the subfamilial placement of the genus Afr. Entomol. 4 1996 111 116
53. D.L.J. Quicke Parasitic Wasps 1997 Chapman & Hall London
54. D.L.J. Quicke, and C. van Achterberg Phylogeny of the subfamilies of the family Braconidae (Hymenoptera) Zool. Verh. Leiden 258 1990 1 95
55. D.L.J. Quicke, C. van Achterberg, and H.C.J. Godfray Comparative morphology of the venom gland and reservoir in opiine and alysiine braconid wasps (Insecta, Hymenoptera, Braconidae) Zool. Scr. 26 1997 23 50
56. D.L.J. Quicke, and R. Belshaw Incongruence between morphological data sets: an example from the evolution of endoparasitism among parasitic wasps (Hymenoptera: Braconidae) Syst. Biol. 48 1999 436 454
57. D.L.J. Quicke, L. Ficken, and M.G. Fitton New diagnostic ovipositor characters for doryctine wasps (Hymenoptera, Braconidae) J. Nat. Hist. 26 1992 1035 1046
58. D.L.J. Quicke, M.G. Fitton, and J. Harris Ovipositor steering mechanisms in braconid wasps J. Hym. Res. 4 1995 110 120
59. D.L.J. Quicke, M.G. Fitton, and S. Ingram Phylogenetic implications of the structure and distribution of ovipositor valvilli in the Hymenoptera J. Nat. Hist. 26 1992 587 608
60. D.L.J Quicke, H.H. Basibuyuk, M.G. Fitton, and A.P. Rasnitsyn Morphological, palaentological and molecular aspects of ichneumonoid phylogeny (Hymenoptera: Insecta) Zool. Scr. 28 1999 175 202
61. D.L.J. Quicke, J. Tunstead, J.V. Falco, and P.M. Marsh Venom gland and reservoir morphology in the Doryctinae and related braconid wasps (Insecta, Hymenoptera, Braconidae) Zool. Scr. 21 1992 403 416
62. D.L.J. Quicke, M.G. Fitton, J.R. Tunstead, S.N. Ingram, and P.V. Gaitens Ovipositor structure and relationships within the Hymenoptera, with special reference to the Ichneumonoidea J. Nat. Hist. 28 1994 635 682
63. H. Rahman, M.G. Fitton, and D.L.J. Quicke Ovipositor internal microsculpture in the Braconidae (Insecta, Hymenoptera) Zool. Scr. 27 1998 319 331
64. A. Rokas, J.A.A. Nylander, F. Ronquist, and G.N. Stone A maximum-likelihood analysis of eight phylogenetic markers in gallwasps (Hymenoptera: Cynipidae): implications for insect phylogenetic studies Mol. Phylogenet. Evol. 22 2002 206 219
65. F. Ronquist, and J.P. Huelsenbeck MrBayes3: Bayesian phylogenetic inference under mixed models Bioinformatics 19 2003 1572 1574
66. D. Scatolini, A.M. Penteado-Dias, and C. van Achterberg Pseudorhysipolis gen. nov. (Hymenoptera: Braconidae: Rhysipolinae), with nine new species from Brazil, Suriname and Panama Zool. Med. Leiden 76 2002 109 131
67. M.J. Sharkey, and D.B. Wahl Cladistics of the Ichneumonoidea (Hymenoptera) J. Hymenopt. Res. 1 1992 15 24
68. M.J. Sharkey Apozyginae R.A. Wharton P.M. Marsh M.J. Sharkey Manual of the New World Genera of the Family Braconidae (Hymenoptera) 1997 International Society of Hymenopterists, Special Publ. 1 Washington, DC 133 134
69. S.R. Shaw, and J.S. Edgerly A new braconid genus (Hymenoptera) parasiting webspinners (Embiidina) in Trinidad Psyche 92 1985 505 511
70. M.R. Shaw, and T. Huddleston Classification and biology of braconid wasps (Hymenoptera: Braconidae) Handbks. Ident. Br. Insect 7 1991 1 126
71. M. Shi, and X. Chen Molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae) based on DNA sequences of 16S rRNA, 18S rDNA and ATPase 6 genes Eur. J. Entomol. 102 2005 133 138
72. Shi, M., Chen, X., Achterberg, C. van. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA, 28S rDNA D2, 18S rDNA gene sequences and morphological characters. Mol. Biol. Evol., in press.
73. H. Shimodaira, and M. Hasegawa Multiple comparisons of log-likelihoods with applications to phylogenetic inference Mol. Biol. Evol. 16 1999 1114 1116
74. M.P. Simmons, and H. Ochoterena Gaps as characters in sequence based phylogenetic analyses Syst. Biol. 49 2000 369 381
75. P.S. Soltis, D.E. Soltis, P.G. Wolf, D.L. Nickrent, S.M. Chaw, and R.L. Chapman The phylogeny of land plants inferred from 18S rDNA sequences: pushing the limits of rDNA signal? Mol. Biol. Evol. 16 1999 1774 1784
76. *: Phylogenetic Analysis Using Parsimony (*and other methods), Version 4.0b10 2002 Sinauer Sunderland, MA
77. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position, specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680
78. V.I. Tobias A new subfamily of braconids (Hymenoptera, Braconidae) from Australia Entomol. Obozr. 67 1988 644 648
79. R.A. Wharton Review of the Hormiini (Hymenoptera: Braconidae) with a description of new taxa J. Nat. Hist. 27 1993 107 171
80. R.A. Wharton Introduction R.A. Wharton P.M. Marsh M.J. Sharkey Manual of the New World Genera of the Family Braconidae (Hymenoptera) 1997 International Society of Hymenopterists, Special Publ. 1 Washington, DC 1 18
81. R.A. Wharton Can braconid classification be restructured to facilitate portrayal of relationships A. Austin M. Dowton Hymenoptera: evolution, biodiversity, and biological control 2000 CSIRO Melbourne 143 153
82. R.A. Wharton, and C. van Achterberg Family group names in Braconidae (Hymenoptera: Ichneumonoidea) J. Hym. Res. 9 2000 254 270
83. R.A. Wharton, and P.E. Hanson Gall wasps in the family Braconidae (Hymenoptera) A. Raman C.W. Schaefer T.M. Withers Biology, Ecology, and Evolution of Gall-inducing Arthropods 2005 Science New Hampshire, USA
84. W.C. Wheeler Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12 1996 1 9
85. W.C. Wheeler Fixed character states and the optimization of molecular sequence data Cladistics 15 1999 379 385
86. W.C. Wheeler, J. Gatesy, and R. DeSalle Elision: a method for accomodating multiple molecular sequence alignments with alignment ambiguous sites Mol. Phylogenet. Evol. 4 1995 1 9
87. J.B. Whitfield The polyphyletic origin of endoparasitism in the cyclostome lineages of Braconidae (Hymenoptera) Syst. Entomol. 17 1992 273 286
88. J.B. Whitfield, and R.A. Wharton Hormiinae R.A. Wharton P.M. Marsh M.J. Sharkey Manual of the New World Genera of the Family Braconidae (Hymenoptera) 1997 International Society of Hymenopterists, Special Publ. 1 Washington, DC 291 307
89. J.B. Whitfield, C. Won-Young, and S. Kyong-In Andesipolis, a puzzling new genus of cyclostome Braconidae (Hymenoptera) from the Chilean Andes, with descriptions of three new species Zootaxa 438 2004 1 15
90. A. Zaldivar-Riverón, B. Areekul, M.R. Shaw, and D.L.J. Quicke Comparative morphology of the venom apparatus in the braconid wasp subfamily Rogadinae (Insecta, Hymenoptera, Braconidae) and related taxa Zool. Scr. 33 2004 223 237
91. D.J. Zwickl, and D.M. Hillis Increased taxon sampling greatly reduces phylogenetic error Syst. Biol. 51 2002 588 598