Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids

BMC Evolutionary Biology

Volumn 11, Issue 1, 2011, Pages

  Sandrock, Christoph ^a,b   Schirrmeister, Bettina E ^a   Vorburger, Christoph ^c,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b AGROSCOPE LIEBEFELD POSIEUX RESEARCH STATION ALP   (Switzerland)

^c ETH ZURICH   (Switzerland)

^d SWISS FEDERAL INSTITUTE OF AQUATIC SCIENCE AND TECHNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

APHID; CRYPSIS; EVOLUTIONARY BIOLOGY; GENEALOGY; GENETIC MARKER; HOST-PARASITOID INTERACTION; INTROGRESSION; PHYLOGENETICS; SPECIALIZATION; TAXONOMY; THELYTOKY; TOPOLOGY; WASP;

EUROPE;

APHIDIDAE; LYSIPHLEBUS FABARUM;

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; APHID; ARTICLE; ASEXUAL REPRODUCTION; EUROPE; FEMALE; GENETIC VARIABILITY; GENETICS; MALE; MOLECULAR EVOLUTION; PHYSIOLOGY;

ANIMALS; APHIDS; DNA, MITOCHONDRIAL; EUROPE; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; MALE; MICROSATELLITE REPEATS; REPRODUCTION, ASEXUAL;

EID: 82355182592     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-11-348     Document Type: Article

References (114)

1. Genomic signatures of ancient asexual lineages. Normark BB, Judson OP, Moran NA, Biological Journal of the Linnean Society 2003 79 1 69 84 (Pubitemid 36590301)
2. Signs of sex: what we know and how we know it. Schurko AM, Neiman M, Logsdon JM, Trends in Ecology & Evolution 2009 24 4 208 217
3. Ancient asexual scandals. Judson OP, Normark BB, Trends in Ecology & Evolution 1996 11 2 41 A46
4. A pluralist approach to sex and recombination. West SA, Lively CM, Read AF, Journal of Evolutionary Biology 1999 12 6 1003 1012 (Pubitemid 29536708)
5. Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Simon JC, Delmotte F, Rispe C, Crease T, Biological Journal of the Linnean Society 2003 79 1 151 163 (Pubitemid 36590308)
6. Ecology and evolution of sex in aphids. Simon JC, Rispe C, Sunnucks P, Trends in Ecology & Evolution 2002 17 1 34 39 (Pubitemid 34076725)
7. Sex determination in the Hymenoptera-a review of models and evidence. Cook JM, Heredity 1993 71 4 421 435
8. Molecular markers indicate rare sex in a predominantly asexual parasitoid wasp. Belshaw R, Quicke DLJ, Völkl W, Godfray HCJ, Evolution 1999 53 4 1189 1199 (Pubitemid 29416960)
9. Biology and distribution of microbe-associated thelytokous populations of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae). Star P, Journal of Applied Entomology 1999 123 4 231 235
10. Cytology and Evolution in Parthenogenesis. Suomalainen E, Saura A, Lokki J, CRC Press Boca Raton, Fla 1987
11. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Stouthamer R, Breeuwer JAJ, Hurst GDD, Annu Rev Microbiol 1999 53 71 102 (Pubitemid 29503726)
12. Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium. Giorgini M, Monti MM, Caprio E, Stouthamer R, Hunter MS, Heredity 2009 102 4 365 371
13. The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. Hagimori T, Abe Y, Date S, Miura K, Curr Microbiol 2006 52 2 97 101 (Pubitemid 43260441)
14. Wolbachia in two insect host-parasitoid communities. West SA, Cook JM, Werren JH, Godfray HCJ, Molecular Ecology 1998 7 11 1457 1465 (Pubitemid 28504063)
15. The cytogenetics of thelytoky in a predominantly asexual parasitoid wasp with covert sex. Belshaw R, Quicke DLJ, Genome 2003 46 1 170 173 (Pubitemid 36463232)
16. Automictic parthenogenesis in the parasitoid Venturia canescens (Hymenoptera: Ichneumonidae) revisited. Beukeboom LW, Pijnacker LP, Genome 2000 43 6 939 944 (Pubitemid 32119804)
17. Single-locus recessive inheritance of asexual reproduction in a parasitoid wasp. Sandrock C, Vorburger C, Current Biology 2011 21 5 433 437
18. A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Lattorff HMG, Moritz RFA, Fuchs S, Heredity 2005 94 5 533 537 (Pubitemid 40641176)
19. The origin and genetic basis of obligate parthenogenesis in Daphnia pulex. Innes DJ, Hebert PDN, Evolution 1988 42 5 1024 1035
20. Evolutionary history of contagious asexuality in Daphnia pulex. Paland S, Colbourne JK, Lynch M, Evolution 2005 59 4 800 813 (Pubitemid 40589290)
21. Loss of sexual reproduction and dwarfing in a small metazoan. Stelzer CP, Schmidt J, Wiedlroither A, S R, PLoS One 2010 5 9 12854
22. Aphid Parasitiods of the Czech Republik. Star P, Academia, Prague, Czech Republik 2006
23. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Kavallieratos NG, Tomanovi Star P, Athanassiou CG, Sarlis GP, Petrovi O, Niketi M, Veroniki MA, Applied Entomology and Zoology 2004 39 3 527 563 (Pubitemid 39483889)
24. Specificity of parasitoids (Hymenoptera, Aphidiidae) to the black bean aphid, Aphis fabae complex, in agroecosystems. Star P, Acta Entomologica Bohemoslovaca 1986 83 1 24 29
25. Evidence for a cryptic species complex in the ant parasitoid Apocephalus paraponerae (Diptera: Phoridae). Morehead SA, Seger J, Feener DH, Brown BV, Evolutionary Ecology Research 2001 3 3 273 284 (Pubitemid 33620349)
26. DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Smith MA, Woodley NE, Janzen DH, Hallwachs W, Hebert PDN, Proceedings of the National Academy of Sciences of the United States of America 2006 103 10 3657 3662 (Pubitemid 43376611)
27. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, Hebert PDN, Proceedings of the National Academy of Sciences of the United States of America 2008 105 34 12359 12364
28. Genetic divergence among host-specific cryptic species in Cotesia melitaearum aggregate (Hymenoptera: Braconidae), parasitoids of checkerspot butterflies. Kankare M, Van Nouhuys S, Hanski I, Annals of the Entomological Society of America 2005 98 3 382 394 (Pubitemid 40707028)
29. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Stireman JO, Nason JD, Heard SB, Seehawer JM, Proceedings of the Royal Society B-Biological Sciences 2006 273 1586 523 530 (Pubitemid 46768055)
30. Spatial and genetic structure of host-associated differentiation in the parasitoid Copidosoma gelechiae. Kolaczan CR, Heard SB, Segraves KA, Althoff DM, Nason JD, Journal of Evolutionary Biology 2009 22 6 1275 1283
31. Phylogeography of a parasitoid wasp (Diaeretiella rapae): no evidence of host-associated lineages. Baer CF, Tripp DW, Bjorksten TA, Antolin MF, Molecular Ecology 2004 13 7 1859 1869 (Pubitemid 38847591)
32. A test of host-associated differentiation across the 'parasite continuum' in the tri-trophic interaction among yuccas, bogus yucca moths, and parasitoids. Althoff DM, Molecular Ecology 2008 17 17 3917 3927
33. Molecular markers reveal strong geographic, but not host associated, genetic differentiation in Aphidius transcaspicus, a parasitoid of the aphid genus Hyalopterus. Lozier JD, Roderick GK, Mills NJ, Bull Entomol Res 2009 99 1 83 96
34. Do parasitoids diversify in response to host-plant shifts by herbivorous insects? Cronin JT, Abrahamson AG, Ecological Entomology 2001 26 4 347 355 (Pubitemid 32781922)
35. Interactions between ants and parasitoid wasps foraging for Aphis fabae spp. cirsiiacanthoidis on thistles. Völkl W, Mackauer M, J Insect Behav 1993 6 3 301 312
36. Chemische Mimikry bei Blattlausparasitoiden der Gattung Lysiphlebus (Hymenoptera, Aphidiidae). Liepert C, PhD Thesis Universität Bayreuth, Germany 1996
37. R: A language and environment for statistical computing. R Development Core Team, 2008 http://cran.r-project.org
38. Statistics: An Introduction using R. Crawley MJ, Cichester: John Wiley & Sons Ltd 2005
39. Microsatellite DNA markers for the aphid parasitoid Lysiphlebus fabarum and their applicability to related species. Sandrock C, Frauenfelder N, von Burg S, Vorburger C, Mol Ecol Notes 2007 7 6 1080 1083 (Pubitemid 350059192)
40. Microsatellite DNA markers for Lysiphlebus testaceipes. Fauvergue X, Tentelier C, Genson G, Audiot P, Guillemaud T, Streiff RJ, Mol Ecol Notes 2005 5 1 109 111 (Pubitemid 40350895)
41. GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Arnaud-Haond S, Belkhir K, Mol Ecol Notes 2007 7 1 15 17 (Pubitemid 46046572)
42. Standardizing methods to address clonality in population studies. Arnaud-Haond S, Duarte CM, Alberto F, Serrao EA, Molecular Ecology 2007 16 24 5115 5139 (Pubitemid 350265252)
43. Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). Dorken ME, Eckert CG, Journal of Ecology 2001 89 3 339 350 (Pubitemid 32540371)
44. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Excoffier L, Laval G, Schneider S, Evol Bioinform 2005 47 50
45. FSTAT (version 2.9.3.2), a program to estimate and test gene diversities and fixation indices. Goudet J, 2001 http://www2.unil.ch/popgen/softwares/fstat. htm
46. Constraints on the evolution of asexual reproduction. Engelstädter J, BioEssays 2008 30 11-12 1138 1150
47. Genetic structure of an aphid studied using microsatellites: cyclic parthenogenesis, differentiated lineages and host specialization. Sunnucks P, De Barro PJ, Lushai G, Maclean N, Hales DF, Molecular Ecology 1997 6 11 1059 1073
48. Tackling the population genetics of clonal and partially clonal organisms. Halkett F, Simon JC, Balloux F, Trends in Ecology & Evolution 2005 20 4 194 201 (Pubitemid 40359266)
49. Analyzing tables of statistical tests. Rice WR, Evolution 1989 43 223 225
50. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek RC, Mol Mar Biol Biotechnol 1994 3 294 299
51. Biological identifications through DNA barcodes. Hebert PDN, Cywinska A, Ball SL, deWaard JR, Proc R Soc Lond Ser B-Biol Sci 2003 270 1512 313 321 (Pubitemid 36228536)
52. Clustal-W-Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Thompson JD, Higgins DG, Gibson TJ, Nucleic Acids Research 1994 22 22 4673 4680 (Pubitemid 24354800)
53. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Hall TA, Nuc Acids Symp Ser 1999 41 95 98
54. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Tamura K, Dudley J, Nei M, Kumar S, Molecular Biology and Evolution 2007 24 8 1596 1599 (Pubitemid 47236692)
55. Nuclear integrations-challenges for mitochondrial-DNA markers. Zhang DX, Hewitt GM, Trends in Ecology and Evolution 1996 11 6 247 251
56. Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Song H, Buhay JE, Whiting MF, Crandall KA, Proceedings of the National Academy of Sciences of the United States of America 2008 105 36 13486 13491
57. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Librado P, Rozas J, Bioinformatics 2009 25 11 1451 1452
58. PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods). Version 4. Swofford DL, Sunderland, Massachusetts: Sinauer Associates 2003
59. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Zwickl DJ, PhD Thesis Austin, TX, USA: The University of Texas, Austin, TX, USA 2006
60. MrBayes 3: Bayesian phylogenetic inference under mixed models. Ronquist F, Huelsenbeck JP, Bioinformatics 2003 19 12 1572 1574 (Pubitemid 37038874)
61. A new method for calculating evolutionary substitution rates. Lanave C, Preparata G, Saccone C, Serio G, Journal of Molecular Evolution 1984 20 1 86 93 (Pubitemid 14116237)
62. The general stochastic-model of nucleotide substitution. Rodriguez F, Oliver JL, Marin A, Medina JR, J Theor Biol 1990 142 4 485 501
63. MODELTEST: testing the model of DNA substitution. Posada D, Crandall KA, Bioinformatics 1998 14 9 817 818 (Pubitemid 28552116)
64. Awty: A system for graphical exploration of mcmc convergence in bayesian phylogenetic inference. Wilgenbusch J, Warren D, Swofford DL, 2004 http://ceb.csit.fsu.edu/awty/
65. Tracer v1.4. Rambaut A, Drummond AJ, 2007 http://tree.bio.ed.ac.uk/ software/tracer/
66. Mesquite: a modular system for evolutionary analysis. v2.71. Maddison WP, Maddison DR, 2009 http://mesquiteproject.org
67. A likelihood approach to estimating phylogeny from discrete morphological character data. Lewis PO, Syst Biol 2001 50 6 913 925
68. TCS: a computer program to estimate gene genealogies. Clement M, Posada D, Crandall KA, Molecular Ecology 2000 9 10 1657 1659
69. The analysis of population survey data on DNA-sequence variation. Lynch M, Crease TJ, Molecular Biology and Evolution 1990 7 4 377 394
70. A statistical test for detecting geographic subdivision. Hudson RR, Boos DD, Kaplan NL, Molecular Biology and Evolution 1992 9 1 138 151
71. Molecular epidemiology of clonal diploids: a quick overview and a short DIY (do it yourself) notice. de Mees T, Lehmann L, Balloux F, Infection Genetics and Evolution 2006 6 2 163 170 (Pubitemid 43285823)
72. Population genetics and molecular epidemiology or how to "débusquer la bête". de Mees T, McCoy KD, Prugnolle F, Chevillon C, Durand P, Hurtrez-Bousses S, Renaud F, Infection Genetics and Evolution 2007 7 2 308 332 (Pubitemid 46172943)
73. GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations (Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)). Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F, 1996
74. Multiple-regression and correlation extensions of the Mantel test of matrix correspondence. Smouse PE, Long JC, Sokal RR, Systematic Zoology 1986 35 4 627 632
75. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Rousset F, Genetics 1997 145 4 1219 1228 (Pubitemid 27149123)
76. A unified approach to the study of hypervariable polymorphisms: statistical considerations of determining relatedness and population distances. Chakraborty R, Jin L, DNA Fingerprinting: State of the Science Basel, Switzerland: Birkhäuser, Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ, 1993 153 175
77. Populations 1.2.30. Langella O, 1999 http://bioinformatics.org/~tryphon/ populations/.
78. Population diversity in deuterotokous Lysiphlebus species, parasitoids of aphids (Hymenoptera, Aphidiidae). Nemec V, Star P, Acta Entomologica Bohemoslovaca 1985 82 3 170 174
79. Spatial population dynamics of a specialist aphid parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae: Aphidiinae): evidence for philopatry and restricted dispersal. Nyabuga FN, Loxdale HD, Heckel DG, Weisser WW, Heredity 2010 105 5 433 442
80. Geographical distribution and genetic relatedness of sympatrical thelytokous and arrhenotokous populations of the parasitoid Venturia canescens (Hymenoptera). Schneider MV, Beukeboom LW, Driessen G, Lapchin L, Bernstein C, van Alphen JJM, Journal of Evolutionary Biology 2002 15 2 191 200 (Pubitemid 34271263)
81. Gene flow between arrhenotokous and thelytokous populations of Venturia canescens (Hymenoptera). Schneider MV, Driessen G, Beukeboom LW, Boll R, van Eunen K, Selzner A, Talsma J, Lapchin L, Heredity 2003 90 3 260 267 (Pubitemid 36412970)
82. Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers. Rey O, Loiseau A, Facon B, Foucaud J, Orivel J, Cornuet JM, Robert S, Dobigny G, Delabie JHC, Dos Santos C, et al. Molecular Biology and Evolution 2011 28 9 2591 2601
83. Diploid males sire triploid daughters and sons in the parasitoid wasp Cotesia vestalis. de Boer JG, Ode PJ, Vet LEM, Whitfield J, Heimpel GE, Heredity 2007 99 3 288 294 (Pubitemid 47295858)
84. Sex determination in the Hymenoptera. Heimpel GE, de Boer JG, Annu Rev Entomol 2008 53 209 230 (Pubitemid 351341939)
85. Contagious parthenogenesis, automixis, and a sex determination meltdown. Engelstädter J, Sandrock C, Vorburger C, Evolution 2011 65 2 501 511
86. The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Storeck A, Poppy GM, van Emden HF, Powell W, Entomologia Experimentalis Et Applicata 2000 97 1 41 46
87. Behavioural differences between Aphidius ervi populations from two tritrophic systems are due to phenotypic plasticity. Daza-Bustamante P, Fuentes-Contreras E, Rodriguez LC, Figueroa CC, Niemeyer HM, Entomologia Experimentalis Et Applicata 2002 104 2-3 321 328 (Pubitemid 36093416)
88. Host-range evolution in Aphidius parasitoids: fidelity, virulence and fitness trade-offs on an ancestral host. Henry LM, Roitberg BD, Gillespie DR, Evolution 2008 62 3 689 699 (Pubitemid 351348260)
89. Ecology of infochemical use by natural enemies in a tritrophic context. Vet LEM, Dicke M, Annu Rev Entomol 1992 37 141 172 (Pubitemid 24406770)
90. Host plant fitness and host acceptance in the aphid parasitoid Lysiphlebus testaceipes (Cresson). Steinberg S, Prag H, Rosen D, Bulletin IOBC wprs 1993 16 161 164
91. Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hymenoptera: Aphidiidae). Weisser WW, Völkl W, Journal of Applied Entomology 1997 121 1 23 28 (Pubitemid 27205110)
92. Host-related fitness trade-offs in a presumed generalist parasitoid, Diaeretiella rapae (Hymenoptera: Aphidiidae). Antolin MF, Bjorksten TA, Vaughn TT, Ecological Entomology 2006 31 3 242 254
93. The potential host ranges in Australia of some imported aphid parasites [Hymenoptera, Ichneumonoidea, Aphidiidae]. Carver M, Entomophaga 1984 29 4 351 359
94. Wirtsbindung der Aphidiinae und Fahrholz'sche Regel. Mackauer M, Verh Int Kongr Entomol Wien, 1960 1962 2
95. La parthénogenèse géographique. Contribution l'étude biologique et cytologique de la parthénogenèse naturelle. Vandel A, Bulletin Biologique de la France et de la Belgique 1928 62 164 281
96. Explaining the geographic distributions of sexual and asexual populations. Peck JR, Yearsley JM, Waxman D, Nature 1998 391 889 892 (Pubitemid 28157665)
97. Differential success in northwards range expansion between ecotypes of the marble gallwasp Andricus kollari: a tale of two lifecycles. Stone G, Atkinson R, Rokas A, Csoka G, Nieves-Aldrey JL, Molecular Ecology 2001 10 3 761 778 (Pubitemid 32406359)
98. The Evolution of Sex. Maynard Smith J, Cambridge: Cambridge University Press 1978
99. The Monopolization Hypothesis and the dispersal-gene flow paradox in aquatic organisms. De Meester L, Gomez A, Okamura B, Schwenk K, Acta Oecol-Int J Ecol 2002 23 3 121 135 (Pubitemid 34793612)
100. Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini. Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC, Molecular Ecology 2008 17 14 3401 3415 (Pubitemid 352030140)
101. A survey of aphid parasitoids in Kahramanmaras, Turkey (Hymenoptera: Braconidae, Aphidiinae; and Hymenoptera: Aphelinidae). Aslan MM, Uygun N, Star P, Phytoparasitica 2004 32 3 255 263 (Pubitemid 38991346)
102. Parasitoid complex (Hymenoptera, Braconidae, Aphidiinae) of Aphis craccivora Koch (Hemiptera: Aphidoidea) in Iran. Rakhshani E, Talebi AA, Kavallieratos NG, Rezwani A, Manzari S, Tomanovi Journal of Pest Science 2005 78 4 193 198 (Pubitemid 43008908)
103. Aphid-parasitoid (Hymenoptera, Braconidae, Aphidiinae) associations on willows and poplars in Iran. Rakhshani E, Talebi AA, Star P, Tomanovi Manzari S, Acta Zool Acad Sci Hung 2007 53 3 281 292 (Pubitemid 350301179)
104. Aphids and parasitoids on willows and poplars in southeastern Europe (Hornoptera: Aphidoidea; Hymenoptera: Braconidae, Aphidiinae). Tomanovi Kavallieratos NG, Star P, Petrovi-Obradovi O, Tomanovi S, Jovanovi S, J Plant Dis Prot 2006 113 4 174 180 (Pubitemid 44259140)
105. Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae. Rokas A, Atkinson RJ, Webster L, Csoka G, Stone GN, Molecular Ecology 2003 12 8 2153 2174 (Pubitemid 36922328)
106. Die europäischen Arten der Gattung Lysiphlebus Förster (Hymenoptera: Braconidae, Aphidiinae). Eine monographische Revision. Mackauer M, Beiträge zur Entomologie 1960 10 582 623
107. Two new Lysiphlebus species from Europe. Star P, Acta Entomologica Bohemoslovaca 1985 82 6 426 430
108. Aphid parasites (Hymenoptera: Aphidiidae) of the Mediterranean area. Star P, Junk, The Hague, The Netherlands 1976
109. Lysiphlebus confusus n.sp. per Lysiphlebus ambiguus sensu Auct. Tremblay E, Eady RD, Boll Lab Entomol Agrar Filippo Silvestri 1978 35 180 184
110. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Hebert PDN, Ratnasingham S, deWaard JR, Proc R Soc Lond Ser B-Biol Sci 2003 270 96 S99
111. Phylogenetic relationships among genera of Aphidiinae (Hymenoptera: Braconidae) based on DNA sequence of the mitochondrial 16S rRNA gene. Kambhampati S, Völkl W, Mackauer M, Systematic Entomology 2000 25 4 437 445
112. A phylogeny of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) inferred from mitochondrial NADH 1 dehydrogenase gene sequence. Smith PT, Kambhampati S, Völkl W, Mackauer M, Mol Phylogenet Evol 1999 11 2 236 245 (Pubitemid 129499263)
113. A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Belshaw R, Quicke DLJ, Mol Phylogenet Evol 1997 7 3 281 293 (Pubitemid 127345891)
114. An 18S rDNA-based molecular phylogeny of Aphidiinae (Hymenoptera: Braconidae). Sanchis A, Latorre A, Gonzalez-Candelas F, Michelena JM, Mol Phylogenet Evol 2000 14 2 180 194 (Pubitemid 30181332)