Comparison of five allopatric fruit fly parasitoid populations (Psyttalia species) (Hymenoptera: Braconidae) from coffee fields using morphometric and molecular methods

Bulletin of Entomological Research

Volumn 98, Issue 1, 2008, Pages 63-75

  Billah, M K ^a   Kimani Njogu, S W ^b   Wharton, R A ^c   Woolley, J B ^c   Masiga, D ^a  

^a INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^b UNIVERSITY OF READING   (United Kingdom)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

AFLP; Allopatric populations; Dendrogram; Genetic distance; Mahalanobis distance; Morphometry; Parasitoids; Phenetic affinity; Psyttalia; Species group

Indexed keywords

PRIMER DNA;

ALLOPATRY; BIOLOGICAL CONTROL; COFFEE; COMPARATIVE STUDY; FLY; MOLECULAR ANALYSIS; MORPHOMETRY; NEW RECORD; PARASITOID; POLYMORPHISM; TWENTIETH CENTURY; WING MORPHOLOGY;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ANIMAL DISEASE; ARTICLE; CHEMISTRY; COFFEE; FEMALE; FORELIMB; GENETIC VARIABILITY; GENETICS; HISTOLOGY; KENYA; LEG; MALE; PARASITOLOGY; PATHOGENICITY; PHYLOGENY; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; TEPHRITIDAE; WASP;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; COFFEA; DNA PRIMERS; FEMALE; KENYA; LOWER EXTREMITY; MALE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRINCIPAL COMPONENT ANALYSIS; TEPHRITIDAE; VARIATION (GENETICS); WASPS; WING;

AFRICA; CAMEROON; EAST AFRICA; GHANA; KENYA; MEDITERRANEAN REGION; MEDITERRANEAN SEA; SUB-SAHARAN AFRICA; WEST AFRICA;

BRACONIDAE; HYMENOPTERA; OPIUS CONCOLOR; PSYTTALIA;

EID: 38549117290     PISSN: 00074853     EISSN: 14752670     Source Type: Journal    
DOI: 10.1017/S000748530700541X     Document Type: Article

References (91)

1. Alvarez, J.M. & Hoy, M.A. (2002) Evaluation of the ribosomal ITS2 DNA sequences in separating closely related populations of the parasitoid Ageniaspis (Hymenoptera: Encyrtidae). Annals of the Entomological Society of America 95, 250-256.
2. Baer, C.F., Tripp, D.W., Bjorksten, A. & Antolin, M.F. (2004) Phylogeography of a parasitoid wasp (Diaretiella rapae): no evidence of host-associated lineages. Molecular Ecology 13, 1859-1869.
3. Baker, D.A., Loxdale, H.D. & Edwards, O.R. (2003) Genetic variation and founder effects in the parasitoid wasp, Diaretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Molecular Ecology 12, 3303-3311.
4. Barari, H., Ferguson, A.W., Piper, R.W., Smith, E., Quicke, D.L.J. & Williams, I.H. (2005) The separation of two hymenopteran parasitoids, Tersilochus obscurator and Tersilochus microgaster (Ichneumonidae), of stem-mining pests of winter oilseed rape using DNA, morphometric and ecological data. Bulletin of Entomological Research 95, 299-307.
5. Bianchi, F.A. & Krauss, N.H. (1937) Fruit fly investigations in East Africa. Hawaiian Planters Record 41, 299-306.
6. Billah, M.K. (2004) Biosystematic studies of Psyttalia species (Hymenoptera: Braconidae): Parasitoids attacking fruit-infesting flies (Diptera: Tephritidae) in Africa. 236 pp. PhD thesis, University of Ghana, Legon-Accra.
7. Billah, M.K., Kimani-Njogu, S., Overholt, W.A., Wharton, R.A., Wilson, D.D. & Cobblah, M.A. (2005) The effect of host larvae on three Psyttalia species (Hymenoptera: Braconidae): parasitoids of fruit-infesting flies (Diptera: Tephritidae). International Journal of Tropical Insect Science 25(3), 168-175.
8. Bokonon-Ganta, A.H., Ramadan, M.M., Wang, X.-G. & Messing, R.H. (2005) Biological performance and potential of Fopius ceratitivorus (Hymenoptera: Braconidae), an egg-larval parasitoid of tephritid fruit flies newly imported to Hawaii. Biological Control 33, 238-247.
9. Bookstein, F.L., Chernoff, B., Elder, R., Humphries, J., Smith, G. & Strauss, R. (1985) Morphometrics in evolutionary biology. The Academy of Natural Science of Philadelphia, Special Publication, No. 15, 277 pp.
10. Brown, J.M., Pellmyr, O., Thompson, J.N. & Harrison, R.G. (1994) Phylogeny of Greya (Lepidoptera: Prodoxidae), based on nucleotide sequence variation in mitochondrial cytochrome oxidase I and II: congruence with morphological data. Molecular Biology and Evolution 11, 128-141.
11. Campbell, B., Heraty, J.M., Rasplus, J.-Y., Chan, K., Stephan-Campbell, J.D. & Babcock, C. (2000) Molecular systematics of the Chalcidoidea using 28S-D2 rDNA. pp. 59-71 in Austin, A.D. & Dowton, M. (Eds) Hymenoptera: Evolution, Biodiversity and Biological Control. Collingwood, Victoria, Australia, CSIRO Publishing.
12. Carmichael, A.E., Wharton, R.A. & Clarke, A.R. (2005) Opiine parasitoids (Hymenoptera: Braconidae) of tropical fruit flies (Diptera: Tephritidae) of the Australian and South Pacific region. Bulletin of Entomological Research 95, 545-569.
13. 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.
14. Chinajariyawong, A., Clark, A.R., Jirasurat, M., Kritsaneepiboon, S., Lahey, H.A., Vijaysegaran, S. & Walter, G.H. (2000) Survey of opiine parasitoids of fruit flies (Diptera: Tephritidae) in Thailand and Malaysia. Raffles Bulletin of Zoology 48, 71-101.
15. Clausen, C.P., Clancy, D.W. & Chock, Q.C. (1965) Biological control of the Oriental fruit fly and other fruit flies in Hawaii. USDA Technical Bulletin, No. 1322.
16. Copeland, R.S., White, I.M., Okumu, M., Machera, P. & Wharton, R.A. (2004) Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bishop Museum Bulletins in Entomology 12, 135-164.
17. Copeland, R.S., Wharton, R.A., Luke, Q., De Meyer, M., Lux, S., Zenz, N., Machera, P. & Okumu, M. (2006) Geographic distribution, host fruit, and parasitoids of African fruit fly pests Ceratitis anonae, Ceratitis cosyra, Ceratitis fasciventris and Ceratitis rosa (Diptera: Tephritidae) in Kenya. Annals of the Entomological Society of America 99(2), 261-278.
18. Delucchi, V. (1957) Les parasites de la mouche des olives. Entomophaga 2, 106-118.
19. Drew, R.A.I., Tsuruta, K. & White, I.M. (2005) A new species of pest fruit fly (Diptera: Tephritidae: Dacinae) from Sri Lanka and Africa. African Entomology 13, 149-154.
20. Fischer, M. (1958) Ueber dei Variabilitaet von Toxonomisch wichtigen merkmalen bei Opius concolor Szepl. (Hymenoptera: Braconidae). Entomophaga 3, 55-66.
21. Fischer, M. (1963) Das Genus Austroopius Szépligeti. Mitteilungen der Zoologie am Museum Berlin 39, 173-186.
22. Fischer, M. (1971) Hym. Braconidae. World Opiinae. Index of Entomophagous Insect. 189 pp. Paris, Le Francois.
23. Fischer, M. (1972) Hymenoptera: Braconidae (Opiinae I). Das Tierreich 91, 1-620.
24. Fischer, M. (1987) Hymenoptera: Opiinae III - äthiopische, orientalische, australische und ozeanische Region. Das Tierreich 104, 1-734.
25. Gillespie, J.J., Munro, J.B., Heraty, J.M., Yoder, M.J., Owen, A.K. & Carmichael, A. (2005) A secondary structural model of the 28S rRNA expansion segments D2 and D3 from chalcidoid wasps (Hymenoptera: Chalcidoidea): Implications for multiple sequence alignment and phylogeny reconstruction. Molecular Biology and Evolution 22, 1593-1608.
26. Greathead, D.J. (1976). Mediterranean fruit fly, Olive fly. pp. 37-43. in Greathead, D. J. (Ed.). A review of biological control in western and southern Europe. Commonwealth Institute of Biological Control Technical Communications 7.
27. Greenstone, M.H. (2006) Molecular methods for assessing insect parasitism. Bulletin of Entomological Research 96, 1-13.
28. Han, J.-Y. & McPheron, B.A. (1997) Molecular phylogenetic study of Tephritidae (Insecta: Diptera) sing partial sequences of the Mitochondrial 16S Ribosomal DNA. Molecular Phylogenetics and Evolution 7(1), 17-32.
29. Heraty, J.M. (2004) Molecular systematics, Chalcidoidea and biological control. pp. 39-71 in Ehler, L.E., Sforza, R. & Mateille, T. (Eds) Genetics, Evolution and Biological Control. London, CAB International.
30. Heraty, J.M. & Woolley, J.B. (1993) Separate species or polymorphism: A recurring problem in Kapala (Hymenoptera: Eucharitidae). Annals of the Entomological Society of America 86(5), 517-531.
31. Hillis, D.M. (1987) Molecular versus morphological approaches to systematics. Annual Review of Ecology and Systematics 18, 23-42.
32. Jolicoeur, P. & Mosimann, J.E. (1960) Size and shape variation in the painted turtle. A principal component analysis. Growth 24, 339-354.
33. Kankare, M., Jensen, M.K., Kester, K.M. & Saccheri, I.J. (2004) Characterization of microsatellite loci in two primary parasitoids of the butterfly Melitaea cinxia, Cotesia melitaearum and Hyposoter horticola (Hymenoptera). Molecular Ecology Notes 4, 231-233.
34. Kazachkova, N., Fahleson, J. & Meijer, J. (2004) Establishment of the Amplified Fragment Length Polymorphism (AFLP) technique for genotyping of pollen beetle (Meligethes aeneus) - a noxious insect pest on oilseed rape (Brassica napus). Molecular Biology Reports 31, 37-42.
35. Kimani-Njogu, S.W. & Wharton, R.A. (2002) Two new species of Opiinae (Hymenoptera: Braconidae) attacking fruit-infesting Tephritidae (Diptera) in western Kenya. Proceedings of the Entomological Society of Washington 104, 79-90.
36. Kimani-Njogu, S.W., Overholt, W.A., Woolley, J.B. & Omwega, C.O. (1998) Electrophoretic and phylogenetic analyses of selected allopatric populations of the Cotesia flavipes complex (Hymenoptera: Braconidae), parasitoids of cereal stem borers. Biochemical Systematics and Ecology 26, 285-296.
37. Kimani-Njogu, S.W., Trostle, M.K., Wharton, R.A., Woolley, J.B. & Raspi, A. (2001) Biosystematics of the Psyttalia concolor species complex (Hymenoptera: Braconidae: Opiinae): the identity of populations attacking Ceratitis capitata (Diptera: Tephritidae) in coffee in Kenya. Biological Control 20, 167-174.
38. Knipling, E.F. (1992) Principles of insect parasitism analyzed from new perspectives - Practical implications for regulating insect populations by biological control means. USDA Agricultural Handbook No. 693, 337 pp.
39. Kumar, S., Tamura, K. & Nei, M. (2004) MEGA 3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Briefings in Bioinformatics 5, 150-163.
40. Landry, B., Powell, J.A. & Sperling, F.A.H. (1999) Systematics of the Argyrotaenia franciscana (Lepidoptera: Tortricidae) species group: evidence from mitochondrial DNA. Annals of the Entomological Society of America 92, 40-46.
41. Loxdale, H.D. & Lushai, G. (1998) Molecular markers in entomology. Bulletin of Entomological Research 88, 577-600.
42. Lux, S.A., Copeland, R.S., White, I.M., Manrakhan, A. & Billah, M.K. (2003) A New Invasive Fruit Fly Species from the Bactrocera dorsalis (Hendel) Group Detected in East Africa. Insect Science and its Application 23(4), 355-361.
43. Machal, P. (1910) Sur un Braconide nouveau, parasite du Dacus oleae. Bulletin de la Société Entomologique de France 1910, 243-244.
44. Marcus, L.F. (1990) Traditional morphometrics. pp. 77-122 in Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2. Ann Arbor, Michigan, University of Michigan. Museum of Zoology.
45. Masaba, D.M., Owuor, J.B.O. & Gathaara, M.P.H. (1986) Arabica coffee production in Kenya: An overview. Outlook on Agriculture 15(2), 88-92.
46. Masiga, D., Tait, A. & Turner, C.M.R. (2000) Amplified Restriction Fragment Length Polymorphism in parasite genetics. Parasitology Today 16(8), 350-353.
47. Messing, R.H., Klungness, L.M., Purcell, M. & Wong, T. (1993) Quality control parameters of mass-reared opiine parasitoids used in augmentative biological control of tephritid fruit flies in Hawaii. Biological Control 3, 140-147.
48. Monastero, S. (1931) Un nuovo parassita endofaga della mosca delle olive trovato in Altavilla Milicia (Silicia). Atti della Reale Accademia della Scienze Palermo 16, 1-6.
49. Monastero, S. (1934) Studio sulla posizione sistematica dell'Opius siculus Monastero endofago della mosca delle olive. Atti della Reale Accademia della Scienze Palermo 18, 371-389.
50. Muesebeck, C.F.W. (1931) Descriptions of a new genus and eight new species of Ichneumon-flies with taxonomic notes. Proceedings of the United States National Museum 76, 1-16.
51. Neff, N.A. & Marcus, L.F. (1980) A Survey of Multivariate Methods for Systematics. 243 pp. New York, Privately Published and A.M.N.H.
52. Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583-590.
53. Oerke, E.-C., Dehne, H-W., Schönbeck, F. & Weber, A. (1994) Crop Production and Crop Protection: Estimated Losses in Major Food and Cash Crops. 808 pp. Amsterdam, Elsevier Science Publishers.
54. Ovruski, S., Aluja, M., Sivinski, J. & Wharton, R.A. (2000) Hymenoptera parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biocontrol. Integrated Pest Management Review 5, 81-107.
55. PopGen 32 (1997) Population Genetic Analysis software, version 1.31. Canada, University of Alberta and Centre for International Forestry Research.
56. Purcell, M., Herr, J.C., Messing, R.H. & Wong, T. (1998) Interactions between augmentatively released Diachasmimorpha longicaudata (Hymenoptera: Braconidae) and a complex of opiine parasitoids in a commercial guava orchard. Biocontrol Science and Technology 8, 139-151.
57. Quicke, D.L.J. (2004) The world of DNA barcoding and morphology - collision or synergism and what of the future. Systematist 23, 8-12.
58. Ramadan, M.M. (2004) Mass-rearing biology of Fopius vandenboschi (Hym: Braconidae). Journal of Applied Entomology 128, 226-232.
59. Reineke, A., Karlovsky, P. & Zebitz, C.P.W. (1999) Amplified fragment length polymorphism analysis of different geographic populations of the gypsy moth, Lymantria dispar (Lepidoptera: Lymantriidae). Bulletin of Entomological Research 89, 79-88.
60. Rohlf, F.J. & Bookstein, F.L. (1987) A comment on shearing as a method for size correction. Systematic Zoology 36, 356-367.
61. Rohlf, F.J. & Bookstein, F.L. (1990) Proceedings of the Michigan Morphometrics Workshop. Special Publication No. 2 (The Blue Book). Ann Arbor, Michigan, University of Michigan, Museum of Zoology.
62. SAS Institute Inc. (2001) SAS/STAT® User's Guide, Version 8.2. Cary, NC, USA.
63. Sheppard, W.S., Steck, G.S. & McPheron, B.A. (1992) Geographic populations of the medfly may be differentiated by mitochondrial DNA variation. Experimentia 48, 1010-1013.
64. Silvestri, F. (1913) Viaggio in Africa per cercave parassiti di mosche dei frutti. Bollettino del Laboratorio di Zoologia Generale e Agraria, Portici 8, 1-164.
65. Silvestri, F. (1914) Report of an expedition to Africa in search of the natural enemies of fruit flies. Hawaiian Board of Agriculture & Forestry Division. Entomological Bulletin 3, 176 pp. (Translation of 1913 report in Italian).
66. Sivinski, J. Vulinec, K. & Aluja, M. (2001) Ovipositor length in a guild of parasitoid (Hymenoptera: Braconidae) attacking Anastrepha species fruit flies (Diptera: Tephritidae) in Southern Mexico. Annals of the Entomological Society of America 94(6), 886-895.
67. Sneath, P.H.A. & Sokal, R.R. (1973) Numerical Taxonomy: The Principles and Practice of Numerical Classification. 573 pp. San Francisco, W. H. Freeman & Co.
68. Sokal, R.R. & Rohlf, F.J. (1995) Biometry: The Principles and Practice of Statistics in Biological Research. 3rd edn. 887 pp. San Francisco, W. H. Freeman & Co.
69. Steck, G.J., Gilstrap, F., Wharton, R.A. & Hart, W.G. (1986) Braconid parasitoids of Tephritidae infesting coffee and other fruits in West-central Africa. Entomophaga 31, 59-67.
70. Szépligeti, G. (1910) Description d'une espéce nouvelle d'Opius (Braconidae) de l'Afrique méridionale. Bollettino del Laboratorio di Zoologia Generale e Agraria Portici 4, 346.
71. Triapitsyn, S.V., Vickerman, D.B., Heraty, J.M. & Logarzo, G.A. (2006) A new species of Gonatocerus (Hymenoptera: Mymaridae) parasitic on proconiine sharpshooters (Hemiptera: Cicadellidae) in the New World. Zootaxa 1158, 55-67.
72. Umphrey, G.J. (1996) Morphometric discrimination among sibling species in the fulva-rudis-texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae). Canadian Journal of Zoology 74(3), 528-559.
73. Unruh, T.R., White, W., Gonzalez, D. & Woolley, J.B. (1989) Genetic relationships among seventeen Aphidius (Hymenoptera: Aphidiidae) populations, including six species. Annals of the Entomological Society of America 82, 754-762.
74. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. & Zabeau, M. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407-4414.
75. Walker, F. (1860) Characters of some apparently undescribed Ceylon Insects. Annals and Magazine of Natural History 3(5), 304-311.
76. Waterhouse, D.F. (1993) Biological Control: Pacific Prospects, Supplement 2. 138 pp. Canberra, Australian Centre for International Agricultural Research (ACIAR).
77. Wharton, R.A. (1987) Changes in nomenclature and classification of some opiine Braconidae (Hymenoptera). Proceedings of the Entomological Society of Washington, 89, 61-73.
78. Wharton, R.A. (1988) Classification of the Braconid subfamily Opiinae (Hymenoptera). The Canadian Entomologist 120, 333-360.
79. Wharton, R.A. (1989) Control; classical biological control of fruit-infesting Tephritidae. pp. 303-313 in Robinson, A.S. & Hooper, G. (Eds) Fruit Flies; their Biology, Natural Enemies and Control. World Crop Pests, 3(B). Amsterdam, Elsevier Science Publishers.
80. Wharton, R.A. (1997a) Generic relationships of opiine Braconidae (Hymenoptera) parasitic on fruit- infesting Tephritidae (Diptera). Contributions of the American Entomological Institute 30, 1-53.
81. Wharton, R.A. (1997b) Subfamily Opiinae. pp. 378-395 in Wharton, R.A., Marsh, P.M. & Sharkey, M.J. (Eds) Manual of the new world Genera of the family Braconidae (Hymenoptera). Washington, D.C., The International Society of Hymenopterists (Special publication, 1).
82. Wharton, R.A. (1999) A review of the Old World genus Fopius Wharton (Hymenoptera: Braconidae: Opiinae), with description of two new species reared from fruit-infesting Tephritidae (Diptera). Journal of Hymenoptera Research 8, 48-64.
83. Wharton, R.A. & Gilstrap, F.E. (1983) Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s. l. (Diptera: Tephritidae). Annals of the Entomological Society of America 76, 721-742.
84. Wharton, R.A., Trostle, M.K., Messing, R.H., Copeland, R.S., Kimani-Njogu, S.W., Lux, S., Overholt, W.A., Mohamed, S. & Sivinski, J. (2000) Parasitoids of medfly, Ceratitis capitata, and related tephritids in Kenyan coffee: a predominantly koinobiont assemblage. Bulletin of Entomological Research 90, 517-526.
85. Wharton, R.A., Yoder, M.J., Gillespie, J.J., Patton, J.C. & Honeycutt, R.L. (2006) Relationships of Exodontiella, a non-alysiine, exodont member of the family Braconidae (Insecta, Hymenoptera). Zoologica Scripta 35, 323-340.
86. White, I.M. & Elson-Harris, M.M. (1992) Fruit Flies of Economic Significance: Their Identification and Bionomics. 602 pp. Wallingford, UK, CAB International.
87. Will, K.W. & Rubinoff, D. (2004) Myth of the molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics 20, 47-55.
88. Willard, H.F. & Mason, A.C. (1937) Parasitization of the Mediterranean fruit fly in Hawaii, 1914-1933. USDA Circular 439, 1-18.
89. Wool, D. & Hales, D.F. (1997) Phenotypic plasticity in Australian cotton aphid (Homoptera: Aphididae): host plant effects on morphological variation. Annals of the Entomological Society of America 90, 316-328.
90. Woolley, J.B. & Browning, H.W. (1987) Morphometric analysis of uniparental Aphytis reared from Chaff scale, Pariatoria pergondii Comstock, on Texas citrus (Hymenoptera: Aphelinidae, Homoptera: Diaspididae). Proceedings of the Entomological Society of Washington 89, 77-94.
91. Woolley, J.B., Rose, M. & Krauter, P. (1994) Morphometric comparisons of Aphytis species in the lingnanensis group (Hymenoptera: Aphelinidae). pp. 223-244 in Rosen, D. (Ed.) Advances in Aphytis Research. Andover, UK, Intercept Ltd.