1932

Abstract

The braconid parasitoid wasp subfamily Microgastrinae is perhaps the most species-rich subfamily of animals on Earth. Despite their small size, they are familiar to agriculturalists and field ecologists alike as one of the principal groups of natural enemies of caterpillars feeding on plants. Their abundance and nearly ubiquitous terrestrial distribution, their intricate interactions with host insects, and their historical association with mutualistic polydnaviruses have all contributed to Microgastrinae becoming a key group of organisms for studying parasitism, parasitoid genomics, and mating biology. However, these rich sources of data have not yet led to a robust genus-level classification of the group, and some taxonomic confusion persists as a result. We present the current status of understanding of the general biology, taxonomic history, diversity, geographical patterns, host relationships, and phylogeny of Microgastrinae as a stimulus and foundation for further study. Current progress in elucidating the biology and taxonomy of this important group is rapid and promises a revolution in the classification of these wasps in the near future.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-020117-043405
2018-01-07
2024-06-19
Loading full text...

Full text loading...

/deliver/fulltext/ento/63/1/annurev-ento-020117-043405.html?itemId=/content/journals/10.1146/annurev-ento-020117-043405&mimeType=html&fmt=ahah

Literature Cited

  1. Arias-Penna DC, Whitfield JB, Hallwachs W, Janzen DH. 1.  2013. Three new species of Wilkinsonellus (Braconidae, Microgastrinae) from the Neotropics, and the first host record for the genus. ZooKeys 302:79–95 [Google Scholar]
  2. Austin AD. 2.  1990. Revision of the enigmatic Australasian genus Miropotes Nixon (Hymenoptera: Braconidae: Microgastrinae), with comments on the phylogenetic importance of the female ovipositor system. Syst. Entomol. 15:43–68 [Google Scholar]
  3. Austin AD, Dangerfield PC. 3.  1992. Synopsis of Australasian Microgastrinae (Hymenoptera: Braconidae), with a key to genera and description of new taxa. Invertebr. Taxon. 6:1–76 [Google Scholar]
  4. Austin AD, Dangerfield PC. 4.  1993. Systematics of Australian and New Guinean Microplitis Foerster and Snellenius Westwood (Hymenoptera: Braconidae: Microgastrinae), with a review of their biology and host relationships. Invertebr. Taxon. 7:1097–166 [Google Scholar]
  5. Banks JC, Whitfield JB. 5.  2006. Dissecting the ancient rapid radiation of microgastrine wasp genera using additional nuclear genes. Mol. Phylogenet. Evol. 41:690–703 [Google Scholar]
  6. Beckage NE. 6.  1997. Parasites and Pathogens: Effects of Host Hormones and Behavior San Diego, CA: Chapman and Hall [Google Scholar]
  7. Beckage NE. 7.  2002. Parasite- and pathogen-mediated manipulation of host hormones and behavior. Hormones, Brain and Behavior 3 D Pfaff, A Arnold, A Etgen, S Fahrbach, R Rubin 281–315 San Diego, CA: Academic [Google Scholar]
  8. Beckage NE, Drezen J-M. 8. , eds. 2012. Parasitoid Viruses: Symbionts and Pathogens Amsterdam: Elsevier [Google Scholar]
  9. Beckage NE, Gelman DB. 9.  2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299–330 [Google Scholar]
  10. Belshaw R, Dowton M, Quicke DLJ, Austin A. 10.  2000. Estimating ancestral geographical distributions: a Gondwanan origin for aphid parasitoids?. Proc. R. Soc. B 267:491–96 [Google Scholar]
  11. Belshaw R, Fitton M, Herniou E, Gimeno C, Quicke DLJ. 11.  1998. A phylogenetic reconstruction of the Ichneumonoidea (Hymenoptera) based on the D2 variable region of 28S ribosomal RNA. Syst. Entomol. 23:109–23 [Google Scholar]
  12. Bézier A, Annaheim M, Herbinière J, Wetterwald C, Gyapay G. 12.  et al. 2009. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323:926–30 [Google Scholar]
  13. Bitra K, Burke GR, Strand MR. 13.  2016. Permissiveness of lepidopteran hosts is linked to differential expression of bracovirus genes. Virology 492:259–72 [Google Scholar]
  14. 14. BOLD (Barcode Life Data Syst.). 2017. Taxonomy browser: Microgastrinae BOLD database Guelph, Ont.: accessed March 31, 2017. http://v4.boldsystems.org/index.php/Taxbrowser_Taxonpage?taxon=microgastrinae&searchTax=Search+Taxonomy [Google Scholar]
  15. Bredlau JP, Mohajer YJ, Cameron TM, Kester KM, Fine ML. 15.  2013. Characterization and generation of male courtship song in Cotesia congregata (Hymenoptera: Braconidae). PLOS ONE 8:e62051 [Google Scholar]
  16. Burke GR, Strand MR. 16.  2014. Systematic analysis of a wasp parasitism arsenal. Mol. Ecol. 23:890–901 [Google Scholar]
  17. Burke GR, Walden K, Whitfeld JB, Robertson HM, Strand MR. 17.  2014. Widespread genome organization of an obligate virus mutualist. PLOS Genet 10:e1004660 [Google Scholar]
  18. Carton Y, Poirié M, Nappi A. 18.  2008. Insect immune resistance to parasitoids. Insect Sci 15:67–87 [Google Scholar]
  19. de Boer J, Ode PJ, Rendahl AK, Vet LEM, Whitfield J, Heimpel GE. 19.  2008. Experimental support for multiple-locus complementary sex determination in the parasitoid Cotesia vestalis. Genetics 180:1525–35 [Google Scholar]
  20. de Boer J, Ode PJ, Vet LEM, Whitfield J. 20.  2007. Complementary sex determination in the parasitoid wasp Cotesia vestalis (C. plutellae). J. Evol. Biol. 20:340–48 [Google Scholar]
  21. de Boer J, Ode PJ, Vet LEM, Whitfield JB, Heimpel GE. 21.  2007. Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. Heredity 99:288–94 [Google Scholar]
  22. Dolphin K, Quicke DLJ. 22.  2001. Estimating the global species richness of an incompletely described taxon: an example using parasitoid wasps (Hymenoptera: Braconidae). Biol. J. Linn. Soc. 73:279–86 [Google Scholar]
  23. Dowton M, Austin AD. 23.  1998. Phylogenetic relationships among the microgastroid wasps (Hymenoptera: Braconidae): combined analysis of 16S and 28S rDNA genes and morphological data. Mol. Phylogenet. Evol. 10:354–66 [Google Scholar]
  24. Dowton M, Austin AD, Antolin MF. 24.  1998. Evolutionary relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA sequences. Insect Mol. Biol. 7:129–50 [Google Scholar]
  25. Dupas S, Wanjiru Gitau C, Branca A, Le Ru BP, Silvain J-F. 25.  2008. Evolution of a polydnavirus gene in relation to parasitoid-host species immune resistance. J. Heredity 99:491–99 [Google Scholar]
  26. Fagan-Jeffries E, Austin AD. 26.  2017. Synopsis of the parasitoid wasp genus Choeras Mason (Hymenoptera: Braconidae: Microgastrinae) in Australasia, with the description of two new species. Austral Entomol In press [Google Scholar]
  27. Fernández-Triana J. 27.  2010. Eight new species and an annotated checklist of Microgastrinae (Hymenoptera: Braconidae) from Canada and Alaska. ZooKeys 63:1–53 [Google Scholar]
  28. Fernández-Triana J, Boudreault C, Buffam J, Mclean R. 28.  2016. A biodiversity hotspot for Microgastrinae (Hymenoptera, Braconidae) in North America: annotated species checklist for Ottawa, Canada. ZooKeys 633:1–93 [Google Scholar]
  29. Fernández-Triana J, Goulet H. 29.  2009. Revision of the genus Philoplitis Nixon (Hymenoptera, Braconidae, Microgastrinae). ZooKeys 20:285–98 [Google Scholar]
  30. Fernández-Triana J, Smith MA, Boudreault C, Goulet H, Hebert PDN. 30.  et al. 2011. A poorly known high-latitude parasitoid wasp community: unexpected diversity and dramatic changes through time. PLOS ONE 6:e23719 [Google Scholar]
  31. Fernández-Triana J, van Achterberg C, Whitfield JB. 31.  2014. Australasian endemic no more: four new species of Miropotes Nixon (Hymenoptera, Braconidae, Microgastrinae), with the first record from the Oriental region. Tijdschr. Entomol. 157:59–77 [Google Scholar]
  32. Fernández-Triana JL, Ward J. 32.  2015. Microgastrine wasps of the world Ottawa, Ont.: accessed March 31, 2017 [Google Scholar]
  33. Fernández-Triana JL, Whitfield JB, Rodriguez JJ, Smith MA, Janzen DH. 33.  et al. 2014. Review of Apanteles sensu stricto (Hymenoptera Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica. ZooKeys 383:1–565 [Google Scholar]
  34. Fernández-Triana JL, Whitfield JB, Smith MA, Kula RR, Hallwachs W, Janzen DH. 34.  2015. Revision of the genera Microplitis and Snellenius (Hymenoptera, Braconidae, Microgastrinae) from Area de Conservacion Guanacaste, Costa Rica, with a key to all species previously described from Mesoamerica. Deutsche Entomol. Z. 62:2137–201 https://doi.org/10.3897/dez.62.5276 [Crossref] [Google Scholar]
  35. Field SA, Keller MA. 35.  1993. Courtship and intersexual signaling in the parasitic wasp Cotesia rubecula (Hymenoptera: Braconidae). J. Insect Behav. 6:737–50 [Google Scholar]
  36. Gupta A, Fernández-Triana JL. 36.  2015. Four new species of the genus Diolcogaster Ashmead, 1900 (Hymenoptera: Braconidae: Microgastrinae) from South East Asia with a key to the Indian species. Syst. Parasitol. 90:285–300 [Google Scholar]
  37. Harvey JA, Kos M, Nakamatsu Y, Tanaka T, Dicke M. 37.  et al. 2008. Do parasitized caterpillars protect their parasitoids from hyperparasitoids? A test of the ‘usurpation hypothesis’. Anim. Behav. 76:701–8 [Google Scholar]
  38. Harvey JA, Tanaka T, Kruidhof M, Vet LEM, Gols R. 38.  2011. The usurpation hypothesis revisited: dying caterpillar repels attack from a hyperparasitoid wasp. Anim. Behav. 81:1281–87 [Google Scholar]
  39. Harvey JA, Visser B, Le Lann C, de Boer J, Ellers J, Gols R. 39.  2014. Convergence and divergence in direct and indirect life-history traits of closely related parasitoids (Braconidae: Microgastrinae). Evol. Biol. 41:134–44 [Google Scholar]
  40. Heimpel GE, de Boer JG. 40.  2008. Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53:209–30 [Google Scholar]
  41. Herniou EA, Huguet E, Theze J, Bézier A, Periquet G, Drezen J-M. 41.  2013. When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Phil. Trans. R. Soc. B 368:20130051 [Google Scholar]
  42. Hoedjes KM, Kruidhof HM, Huigens ME, Dicke M, Vet LEM, Smid HM. 42.  2011. Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc. R. Soc. B 278:889–97 [Google Scholar]
  43. Hrcek J, Miller SE, Whitfield JB, Shima H, Novotny V. 43.  2013. Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest. Oecologia 173:521–32 [Google Scholar]
  44. Jancek S, Bezier A, Gayral P, Paillusson C, Kaiser L. 44.  et al. 2013. Adaptive selection on bracovirus genes drives the specialization of Cotesia parasitoid wasps. PLOS ONE 8:e64432 [Google Scholar]
  45. Janzen DH, Hallwachs W. 45.  2016. DNA barcoding the Lepidoptera inventory of a large complex tropical conserved wildland, Area de Conservación Guanacaste, northwestern Costa Rica. Genome 59:641–60 [Google Scholar]
  46. Janzen DH, Hallwachs W, Blandin P, Burns JM, Cadiou JM. 46.  et al. 2009. Integration of DNA barcoding into an ongoing inventory of tropical complex biodiversity. Mol. Ecol. Res. 9:Suppl. 11–26 [Google Scholar]
  47. Jervis MA, Kidd NAC, Fitton MG, Huddleston T, Dawah HA. 47.  1993. Flower-visiting by hymenopteran parasitoids. J. Nat. Hist. 27:67–105 [Google Scholar]
  48. Jones OR, Purvis A, Baumgart E, Quicke DLJ. 48.  2009. Using taxonomic revision data to estimate the geographic and taxonomic distribution of undescribed species richness in the Braconidae (Hymenoptera: Ichneumonoidea). Insect Conserv. Divers. 2:204–12 [Google Scholar]
  49. Kittel RG, Austin AD, Klopfstein S. 49.  2016. Molecular and morphological phylogenetics of chelonine parasitoid wasps (Hymenoptera: Braconidae), with a critical assessment of divergence time estimations. Mol. Phylogenet. Evol. 101:224–41 [Google Scholar]
  50. Kotenko AG. 50.  2007. Microgastrinae. Key to the Insects of Russia Far East. Vol. IV. Neuropteroidea, Mecoptera, Hymenoptera. Pt. 5 AS Lelej 134–92 Vladivostok, Russ.: Dalnauka [Google Scholar]
  51. Kruidhof HM, de Rijk M, Hoffman D, Harvey JA, Vet LEM, Soler Gamborena R. 51.  2013. Effect of belowground herbivory on parasitoid associative learning of plant odors. Oikos 122:1094–100 [Google Scholar]
  52. Kruidhof HM, Pashalidou FG, Fatouros NE, Figueroa IA, Vet LEM. 52.  et al. 2012. Reward value determines memory consolidation in parasitic wasps. PLOS ONE 7:e39615 [Google Scholar]
  53. Le Corff J, Marquis RJ, Whitfield JB. 53.  2000. Temporal and spatial variation in a parasitoid community associated with the herbivores that feed on Missouri Quercus. Environ. Entomol. 29:181–94 [Google Scholar]
  54. Lemmon AR, Emme S, Lemmon EM. 54.  2012. Anchored hybrid enrichment for massively high-throughput phylogenomics. Syst. Biol. 61:727–44 [Google Scholar]
  55. Lemmon EM, Lemmon AR. 55.  2013. High-throughput genomic data in systematics and phylogenetics. Annu. Rev. Ecol. Evol. Syst. 44:99–121 [Google Scholar]
  56. Maeto K. 56.  1996. Intergeneric variation in the external male genitalia of the subfamily Microgastrinae (Hymenoptera, Braconidae), with a reassessment of Mason's tribal system. J. Hymenopt. Res. 5:38–52 [Google Scholar]
  57. Mardulyn P, Whitfield JB. 57.  1999. Phylogenetic siugnal in the COI, 16S, and 28S genes for inferring relationships among genera of Microgastrinae (Hymenoptera: Braconidae). Evidence of a high diversification rate in this group of parasitoids. Mol. Phylogenet. Evol. 12:282–94 [Google Scholar]
  58. Mason WRM. 58.  1981. The polyphyletic nature of Apanteles Foerster (Hymenoptera: Braconidae): a phylogeny and reclassification of Microgastrinae. Mem. Entomol. Soc. Can. 115:1–147 [Google Scholar]
  59. Michel-Salzat A, Whitfield JB. 59.  2004. Preliminary evolutionary relationships within the parasitoid wasp genus Cotesia (Hymenoptera: Braconidae: Microgastrinae): combined analysis of four genes. Syst. Entomol. 29:371–82 [Google Scholar]
  60. Mirarab S, Bayzid MS, Warnow T. 60.  2014. Evaluating summary methods for multilocus species tree estimation in the presence of incomplete lineage sorting. Syst. Biol. 65:366–80 [Google Scholar]
  61. Muirhead KA, Murphy NP, Sallam MN, Donnellan SC, Austin AD. 61.  2006. Genetic variation in the Cotesia flavipes complex of parasitic wasps (Hymenoptera: Ichneumonoidea: Braconidae): towards the effective control of stemborer pests in Australia. Ann. Soc. Entomol. Fr. 42:309–18 [Google Scholar]
  62. Muirhead KA, Murphy NP, Sallam N, Donnellan SC, Austin AD. 62.  2012. Phylogenetics and genetic diversity of the Cotesia flavipes complex of parasitoid wasps (Hymenoptera: Braconidae), biological control agents of lepidopteran stemborers. Mol. Phylogenet. Evol. 63:904–14 [Google Scholar]
  63. Murphy N, Banks JC, Whitfield JB, Austin AD. 63.  2008. Phylogeny of the microgastroid complex of subfamilies of braconid parasitoid wasps based on sequence data from 7 genes, with an improved estimate of the origin of the lineage. Mol. Phylogenet. Evol. 47:378–95 [Google Scholar]
  64. Nixon GEJ. 64.  1965. A reclassification of the tribe Microgasterini (Hymenoptera: Braconidae). Bull. Br. Mus. (Nat. Hist.) Entomol. 2:Suppl.1–284 [Google Scholar]
  65. Nixon GEJ. 65.  1972. A revision of the north-western European species of the laevigatus-group of Apanteles Förster (Hymenoptera, Braconidae). Bull. Entomol. Res. 61:701–43 [Google Scholar]
  66. Papp J. 66.  1988. A survey of the European species of Apanteles Först. (Hymenoptera, Braconidae: Microgastrinae). 11. “Homologization” of the species-groups of Apanteles s.l. with Mason's generic taxa. Checklist of genera. Parasitoid/host list 1. Ann. Hist. Nat. Mus. Natl. Hung. 80:145–75 [Google Scholar]
  67. Pichon A, Bézier A, Urbach S, Aury J-M, Jouan V. 67.  et al. 2015. Recurrent DNA virus domestication leading to different parasite virulence strategies. Sci. Adv. 1:e1501150 [Google Scholar]
  68. Pitz K, Dowling APG, Sharanowski BJ, Boring CAB, Seltmann KC, Sharkey MJ. 68.  2007. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea) as proposed by Shi et al.: a reassessment. Mol. Phylogenet. Evol. 43:338–43 [Google Scholar]
  69. Porter K. 69.  1983. Mulitvoltinism in Apanteles bignellii and the influence of weather on synchronization with its host Euphydryas aurinia. Entomol. Exp. Appl. 34:55–162 [Google Scholar]
  70. Quicke DLJ. 70.  2015. The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology Oxford: Wiley-Blackwell [Google Scholar]
  71. Quicke DLJ, Shaw MR, Takahashi M, Yanechin B. 71.  2004. Cocoon silk chemistry of non-cyclostome Braconidae, with remarks on phylogenetic relationships within the Microgastrinae (Hymenoptera: Braconidae). J. Nat. Hist. 38:2167–81 [Google Scholar]
  72. Quicke DLJ, van Achterberg C. 72.  1990. Phylogeny of the subfamilies of the family Braconidae (Hymenoptera: Ichneumonoidea). Zool. Verh. 258:1–95 [Google Scholar]
  73. Rodriguez JJ, Fernández Triana J, Whitfield JB, Smith MA, Erwin TL. 73.  2013. Extrapolations from field studies and known faunas converge on much higher estimates of world microgastrine parasitoid wasp species richness. Insect Conserv. Diversity 6:530–36 [Google Scholar]
  74. Ruberson JR, Whitfield JB. 74.  1996. Facultative egg-larval parasitism of the beet armyworm, Spodopteraexigua (Lepidoptera: Noctuidae) by Cotesia marginiventris (Hymenoptera: Braconidae). Fla. Entomol. 79:296–302 [Google Scholar]
  75. Saeed A, Austin AD, Dangerfield PC. 75.  1999. Systematics and host relationships of Australasian Diolcogaster (Hymenoptera: Braconidae: Microgastrinae). Invertebr. Taxon. 13:117–78 [Google Scholar]
  76. Schmidt O, Theopold U, Strand M. 76.  2001. Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 23:344–51 [Google Scholar]
  77. Serbielle C, Chowdhury S, Pichon S, Dupas S, Lesobre J. 77.  et al. 2008. Viral cystatin evolution and three-dimensional structure modelling: a case of directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biol 6:38 [Google Scholar]
  78. Serbielle C, Dupas S, Perdereau E, Héricourt F, Dupuy C. 78.  et al. 2012. Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases. BMC Evol. Biol. 12:253 [Google Scholar]
  79. Sharanowski BJ, Dowling APG, Sharkey MJ. 79.  2011. Molecular phylogenetics of Braconidae (Hymenoptera: Ichneumonoidea), based on multiple nuclear genes, and implications for classification. Syst. Entomol. 36:549–72 [Google Scholar]
  80. Shaw MR, Huddleston T. 80.  1991. Classification and Biology of Braconid Wasps (Hymenoptera: Braconidae) Handb. Identif. Brit. Insects Vol. 7, Part 11 London: R. Entomol. Soc. London [Google Scholar]
  81. Shi M, Chen XX, van Achterberg C. 81.  2005. Phylogenetic relationships among the Braconidae (Hymenoptera: Ichneumonoidea) inferred from partial 16S rDNA, 28S rDNA D2, 18S rDNA gene sequences and morphological characters. Mol. Phylogenet. Evol. 37:104–16 [Google Scholar]
  82. Smith MA, Bertrand C, Crosby K, Eveleigh ES, Fernandez-Triana J. 82.  et al. 2012. Wolbachia and DNA barcoding insects: patterns, potential, and problems. PLOS ONE 7:e36514 [Google Scholar]
  83. Smith MA, Fernández-Triana J, Eveleigh E, Gómez JG, Guclu C. 83.  et al. 2012. DNA barcoding and the taxonomy of Microgastrinae wasps (Hymenoptera, Braconidae): impacts after 8 years and nearly 20 000 sequences. Mol. Ecol. Res. 13:168–76 [Google Scholar]
  84. Smith MA, Rodriguez JJ, Whitfield JB, Janzen DH, Hallwachs W. 84.  et al. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology and collections. PNAS 105:12359–64 [Google Scholar]
  85. Song S-N, He J-H, Chen X-X. 85.  2014. The subgenus Choeras Mason, 1981 of genus Apanteles Foerster, 1862 (Hymenoptera, Braconidae, Microgastrinae) from China, with descriptions of eighteen new species. Zootaxa 3754:501–54 [Google Scholar]
  86. Strand MR, Burke GR. 86.  2012. Polydnaviruses as symbionts and gene delivery systems. PLOS Pathog 8:e1002757 [Google Scholar]
  87. Strand MR, Burke GR. 87.  2014. Polydnaviruses: nature's genetic engineers. Annu. Rev. Virol. 1:333–54 [Google Scholar]
  88. Valerio AA, Whitfield JB. 88.  2005. Two new species of the genus Austrocotesia Austin & Dangerfield (Hymnenoptera: Braconidae) from the Andean region of South America. Zootaxa 888:1–11 [Google Scholar]
  89. Valerio AA, Whitfield JB. 89.  2015. Taxonomic review of the genus Hypomicrogaster Ashmead (Hymenoptera: Braconidae: Microgastrinae), with descriptions of 40 new species. Zootaxa 3979:1–98 [Google Scholar]
  90. van Achterberg C. 90.  2003. Western Palaearctic genera of the subfamily Microgastrinae: a reappraisal of the generic and tribal division (Hymenoptera: Braconidae). Parasitic Wasps: Evolution, Systematics, Biodiversity and Biological Control G Melika, G Thuroczy 19–35 Budapest, Hung.: Agroinform [Google Scholar]
  91. van Achterberg C, Quicke DLJ. 91.  1992. Phylogeny of the subfamilies of the family Braconidae: a reassessment assessed. Cladistics 8:1–95 [Google Scholar]
  92. van den Berg M, Verbaarshot PGH, Hontelez S, Vet LEM, Dicke M, Smid HM. 92.  2010. CREB expression in the brains of two closely related parasitic wasp species that differ in long-term memory formation. Insect Mol. Biol. 19:367–79 [Google Scholar]
  93. van Vugt JJFA, Hoedjes KM, van de Geest HC, Schijlen EWGM, Vet LEM, Smid HM. 93.  2015. Differentially expressed genes linked to natural variation in long-term memory formation in Cotesia parasitic wasps. Front. Behav. Neurosci. 9:255 [Google Scholar]
  94. Walker AK, Kitching IJ, Austin AD. 94.  1990. A reassessment of the phylogenetic relationships within the Microgastrinae (Hymenoptera: Braconidae). Cladistics 6:291–306 [Google Scholar]
  95. Wharton RA, Shaw SR, Sharkey MJ, Wahl DB, Woolley JB. 95.  et al. 1992. Phylogeny of the subfamilies of the family Braconidae (Hymenoptera: Ichneumonoidea): a reassessment. Cladistics 8:199–235 [Google Scholar]
  96. Whitfield JB. 96.  1987. Male swarming by a microgastrine braconid, Apanteles coniferae (Haliday) (Hymenoptera). Proc. Trans. Brit. Entomol. Nat. Hist. Soc. 20:133–35 [Google Scholar]
  97. Whitfield JB. 97.  1997. Subfamily Microgastrinae. Identification Manual to the New World Genera of the Family Braconidae (Hymenoptera) RA Wharton, PM Marsh, MJ Sharkey 333–64 Washington, DC: Int. Soc. Hymenopt. [Google Scholar]
  98. Whitfield JB. 98.  2002. Estimating the age of the polydnavirus/braconid wasp symbiosis. PNAS 99:7508–13 [Google Scholar]
  99. Whitfield JB, Kjer KM. 99.  2008. Ancient rapid radiations of insects: challenges for phylogenetic analysis. Annu. Rev. Entomol. 53:449–72 [Google Scholar]
  100. Whitfield JB, Lockhart PJ. 100.  2007. Deciphering ancient rapid radiations. TREE 22:258–65 [Google Scholar]
  101. Whitfield JB, Mardulyn P, Austin AD, Dowton M. 101.  2002. Phylogenetic relationships among microgastrine braconid wasp genera based on data from the 16S, COI and 28S genes and morphology. Syst. Entomol. 27:337–59 [Google Scholar]
  102. Whitfield JB, Marquis RJ, Le Corff J. 102.  1999. Host associations of braconid parasitoids (Hymenoptera: Braconidae) reared from Lepidoptera feeding on oaks (Quercus spp.) in the Missouri Ozarks. Entomol. News 110:225–30 [Google Scholar]
  103. Whitfield JB, Rodriguez JJ, Masonick PK. 103.  2009. Reared microgastrine wasps (Hymenoptera: Braconidae) from Yanayacu Biological Station and environs (Napo Province, Ecuador): diversity and host specialization. J. Insect Sci. 9:31 [Google Scholar]
  104. Williams DJM. 104.  1985. The New World genus Lathrapanteles n. gen.: phylogeny and placement in the Microgastrinae (Hymenoptera: Braconidae: Cotesiini). Can. J. Zool. 63:1962–81 [Google Scholar]
  105. Williams DJM. 105.  1988. Classification, phylogeny and zoogeographic studies of species of Sathon Mason (Hymenoptera: Braconidae). Quaestiones Entomol 24:529–639 [Google Scholar]
  106. Yu DSK, van Achterberg C, Horstmann K. 106.  2005. World Ichneumonoidea 2004. Taxonomy, Biology, Morphology and Distribution CD/DVD Vancouver, Can.: Taxapad [Google Scholar]
  107. Yu DSK, van Achterberg C, Horstmann K. 107.  2012. Taxapad 2012, Ichneumonoidea 2011 Database Ottawa, Can.: accessed March 31, 2017. http://www.taxapad.com [Google Scholar]
  108. Yu DSK, van Achterberg C, Horstmann K. 108.  2016. Taxapad 2016, Ichneumonoidea 2015 Database Ottawa, Can.: accessed March 31, 2017. http://www.taxapad.com [Google Scholar]
/content/journals/10.1146/annurev-ento-020117-043405
Loading
/content/journals/10.1146/annurev-ento-020117-043405
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error