Biological control is widely successful at controlling pests, but effective biocontrol agents are now more difficult to import from countries of origin due to more restrictive international trade laws (the Nagoya Protocol). Coupled with increasing demand, the efficacy of existing and new biocontrol agents needs to be improved with genetic and genomic approaches. Although they have been underutilised in the past, application of genetic and genomic techniques is becoming more feasible from both technological and economic perspectives. We review current methods and provide a framework for using them. First, it is necessary to identify which biocontrol trait to select and in what direction. Next, the genes or markers linked to these traits need be determined, including how to implement this information into a selective breeding program. Choosing a trait can be assisted by modelling to account for the proper agro-ecological context, and by knowing which traits have sufficiently high heritability values. We provide guidelines for designing genomic strategies in biocontrol programs, which depend on the organism, budget, and desired objective. Genomic approaches start with genome sequencing and assembly. We provide a guide for deciding the most successful sequencing strategy for biocontrol agents. Gene discovery involves quantitative trait loci analyses, transcriptomic and proteomic studies, and gene editing. Improving biocontrol practices includes marker-assisted selection, genomic selection and microbiome manipulation of biocontrol agents, and monitoring for genetic variation during rearing and post-release. We conclude by identifying the most promising applications of genetic and genomic methods to improve biological control efficacy.

Animal Breeding and Genomics Wageningen University and Research PO Box 338 6700 AH Wageningen The Netherlands

Biosystematics Group Wageningen University and Research Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands

CABI Rue des Grillons 1 2800 Delémont Switzerland

cE3c Centre for Ecology Evolution and Environmental Changes Faculdade de Ciências da Universidade de Lisboa Edifício C2 Campo Grande 1749 016 Lisbon Portugal

Department of Biochemistry and Biotechnology University of Thessaly Biopolis 41500 Larissa Greece

Department of Biology University of Rochester Rochester NY 14627 USA

Department of Genetics Estructura de Recerca Interdisciplinar en Biotecnología i Biomedicina Unidad Mixta Gestión Biotecnológica de Plagas UV IVIA Universitat de València Dr Moliner 50 46100 Burjassot Valencia Spain

Faculty of Science University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

Groningen Institute for Evolutionary Life Sciences University of Groningen PO Box 11103 9700 CC Groningen The Netherlands

Group for Population and Evolutionary Ecology FB 02 Institute of Ecology University of Bremen Leobener Str 5 28359 Bremen Germany

INRA CNRS UMR 1355 7254 400 Route des Chappes BP 167 06903 Sophia Antipolis Cedex France

Insect Pest Control Laboratory Joint FAO IAEA Division of Nuclear Techniques in Food and Agriculture Vienna International Centre P O Box 100 1400 Vienna Austria

Institut de Recherche en Biologie Végétale Université de Montréal 4101 Sherbrooke Est Montréal Quebec Canada H1X 2B2

Institut für Populationsgenetik Vetmeduni Vienna Veterinärplatz 1 1210 Vienna Austria

Institute of Entomology Biology Centre CAS Branišovská 31 370 05 České Budějovice Czech Republic

Instituto Valenciano de Investigaciones Agrarias Centro de Protección Vegetal y Biotecnología Unidad Mixta Gestión Biotecnológica de Plagas UV IVIA Carretera CV 315 Km 10'7 46113 Moncada Valencia Spain

Kearney Agricultural Research and Extension Center University of California Berkeley 9240 South Riverbend Avenue Parlier CA 93648 USA

Koppert Biological Systems Veilingweg 14 2651 BE Berkel en Rodenrijs The Netherlands

Laboratory of Entomology Wageningen University and Research Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands

Laboratory of Genetics Wageningen University and Research Droevendaalsesteeg 1 6708 PB Wageningen The Netherlands

Netherlands Institute of Ecology Droevendaalsesteeg 10 6708 PB Wageningen The Netherlands

Vienna Graduate School of Population Genetics Vetmeduni Vienna Veterinärplatz 1 1210 Vienna Austria

See more in PubMed

Abe, J. & Pannebakker, B. A. (2017). Development of microsatellite markers and estimation of inbreeding frequency in the parasitoid wasp Melittobia . Scientific Reports 7, 39879. PubMed PMC

Alphey, N. & Bonsall, M. B. (2018). Genetics‐based methods for agricultural insect pest management. Agricultural and Forest Entomology 20, 131–140. PubMed PMC

Ami, E. B. , Yuval, B. & Jurkevitch, E. (2010). Manipulation of the microbiota of mass‐reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. ISME Journal 4, 28–37. PubMed

Andersson, L. , Haley, C. S. , Ellegren, H. , Knott, S. A. , Johansson, M. , Andersson, K. , Andersson‐Eklund, L. , Edfors‐Lilja, I. , Fredholm, M. , Hansson, I. , et al. (1994). Genetic mapping of quantitative trait loci for growth and fatness in pigs. Science 263, 1771–1774. PubMed

Ashley, E. A. (2016). Towards precision medicine. Nature Reviews Genetics 17, 507–522. PubMed

Audsley, M. D. , Ye, Y. H. & McGraw, E. A. (2017). The microbiome composition of Aedes aegypti is not critical for Wolbachia‐mediated inhibition of dengue virus. PLoS Neglected Tropical Diseases 11, e0005426. PubMed PMC

Baird, N. A. , Etter, P. D. , Atwood, T. S. , Currey, M. C. , Shiver, A. L. , Lewis, Z. A. , Selker, E. U. , Cresko, W. A. & Johnson, E. A. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3, e3376. PubMed PMC

Baker, D. A. , Loxdale, H. D. & Edwards, O. R. (2003). Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (M'intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent. Molecular Ecology 12, 3303–3311. PubMed

Baker, B. P. , Green, T. A. & Loker, A. J. (2020). Biological control and integrated pest management in organic and conventional systems. Biological Control 140, 104095.

Bale, J. , van Lenteren, J. & Bigler, F. (2008). Biological control and sustainable food production. Philosophical Transactions of the Royal Society B: Biological Sciences 363, 761–776. PubMed PMC

Bastide, H. , Betancourt, A. , Nolte, V. , Tobler, R. , Stöbe, P. , Futschik, A. & Schlötterer, C. (2013). A genome‐wide, fine‐scale map of natural pigmentation variation in Drosophila melanogaster . PLoS Genetics 9, e1003534. PubMed PMC

Behrens, D. , Huang, Q. , Geßner, C. , Rosenkranz, P. , Frey, E. , Locke, B. , Moritz, R. F. A. & Kraus, F. B. (2011). Three QTL in the honey bee Apis mellifera L. suppress reproduction of the parasitic mite Varroa destructor . Ecology and Evolution 1, 451–458. PubMed PMC

Benoist, R. , Chantre, C. , Capdevielle‐Dulac, C. , Bodet, M. , Mougel, F. , Calatayud, P. A. , Dupas, S. , Huguet, E. , Jeannette, R. , Obonyo, J. , Odorico, C. , Silvain, J. F. , Le Ru, B. & Kaiser, L. (2017). Relationship between oviposition, virulence gene expression and parasitism success in Cotesia typhae nov. sp. parasitoid strains. Genetica 145, 469–479. PubMed

Bentley, D. R. (2006). Whole‐genome re‐sequencing. Current Opinion in Genetics and Development 16, 545–552. PubMed

van den Berg, M. , Duivenvoorde, L. , Wang, G. , Tribuhl, S. , Bukovinszky, T. , Vet, L. E. M. , Dicke, M. & Smid, H. M. (2011). Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps. Animal Behaviour 81, 325–333.

Beukeboom, L. W. & Zwaan, B. J. (2007). Genetics In Insects as Natural Enemies, pp. 167–218. Springer Netherlands, Dordrecht.

Beukeboom, L. W. , Niehuis, O. , Pannebakker, B. A. , Koevoets, T. , Gibson, J. D. , Shuker, D. M. , van de Zande, L. & Gadau, J. (2010). A comparison of recombination frequencies in intraspecific versus interspecific mapping populations of Nasonia . Heredity 104, 302–309. PubMed

Bielza, P. , Balanza, V. , Cifuentes, D. & Mendoza, J. E. (2020). Challenges facing arthropod biological control: identifying traits for genetic improvement of predators in protected crops. Pest Management Science. 10.1002/ps.5857. PubMed DOI

Blossey, B. & Skinner, L. (1999). Design and importance of post‐release monitoring. In Proceedings of the X International Symposium on Biological Control of Weeds, pp. 4–10.

Blum, J. E. , Fischer, C. N. , Miles, J. & Handelsman, J. (2013). Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster . MBio 4, e00860–e00813. PubMed PMC

Bochdanovits, Z. & de Jong, G. (2004). Antagonistic pleiotropy for life–history traits at the gene expression level. Proceedings of the Royal Society of London, Series B: Biological Sciences 271, S75–S78. PubMed PMC

Bon, M. C. , Jones, W. , Hurard, C. , Ris, N. , Pickett, C. , Estoup, A. & Fauvergue, X. (2008). Identification of 21 polymorphic microsatellites in the African parasitoid wasp, Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae). Molecular Ecology Resources 8, 930–932. PubMed

van den Bosch, R. (1971). Biological control of insects. Annual Review of Ecology and Systematics 2, 45–66.

Bourtzis, K. , Nirgianaki, A. , Markakisa, G. & Savakis, C. (1996). Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144, 1063–1073. PubMed PMC

Breeuwer, J. A. J. & Werren, J. H. (1995). Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes. Evolution 49, 705–717. PubMed

Brinker, P. , Fontaine, M. C. , Beukeboom, L. W. & Falcao Salles, J. (2019). Host, symbionts, and the microbiome: the missing tripartite interaction. Trends in Microbiology 27, 480–488. PubMed

Brown, P. M. J. , Ingels, B. , Wheatley, A. , Rhule, E. L. , de Clercq, P. , van Leeuwen, T. & Thomas, A. (2014). Intraguild predation by Harmonia axyridis (Coleoptera: Coccinellidae) on native insects in Europe: molecular detection from field samples. Entomological Science 18, 130–133.

Burr, B. , Burr, F. A. , Thompson, K. H. , Albertson, M. C. & Stuber, C. W. (1988). Gene mapping with recombinant inbreds in maize. Genetics 118, 519–526. PubMed PMC

Callaway, E. (2018). CRISPR plants now subject to tough GM laws in European Union. Nature 560, 16. PubMed

de Clercq, P. , Vandewalle, M. & Tirry, L. (1998). Impact of inbreeding on performance of the predator Podisus maculiventris . BioControl 43, 299–310.

de Clercq, P. , Mason, P. G. & Babendreier, D. (2011). Benefits and risks of exotic biological control agents. BioControl 56, 681–698.

Cock, M. J. W. , van Lenteren, J. C. , Brodeur, J. , Barratt, B. I. P. , Bigler, F. , Bolckmans, K. , Cônsoli, F. L. , Haas, F. , Mason, P. G. & Parra, J. R. P. (2010). Do new access and benefit sharing procedures under the convention on Biological diversity threaten the future of biological control? BioControl 55, 199–218.

Coelho, A. , Rugman‐Jones, P. F. , Reigada, C. , Stouthamer, R. & Parra, J. R. P. (2016). Laboratory performance predicts the success of field releases in inbred lines of the egg parasitoid Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). PLoS One 11, e0146153. PubMed PMC

Colinet, H. , Nguyen, T. T. A. , Cloutier, C. , Michaud, D. & Hance, T. (2007). Proteomic profiling of a parasitic wasp exposed to constant and fluctuating cold exposure. Insect Biochemistry and Molecular Biology 37, 1177–1188. PubMed

Colombari, F. & Battisti, A. (2016). Native and introduced parasitoids in the biocontrol of Dryocosmus kuriphilus in Veneto (Italy). EPPO Bulletin 46, 275–285.

Cong, L. , Chen, F. , Yu, S. , Ding, L. , Yang, J. , Luo, R. , Tian, H. , Li, H. , Liu, H. & Ran, C. (2016). Transcriptome and difference analysis of fenpropathrin resistant predatory mite, Neoseiulus barkeri (Hughes). International Journal of Molecular Sciences 17, 15–17. PubMed PMC

Cook, N. , Trivedi, U. , Pannebakker, B. A. , Blaxter, M. , Ritchie, M. G. , Tauber, E. , Sneddon, T. & Shuker, D. M. (2015). Oviposition but not sex allocation is associated with transcriptomic changes in females of the parasitoid wasp Nasonia vitripennis . G3 Genes|Genomes|Genetics 5, 2885–2892. PubMed PMC

Coombs, E. M. & McEvoy, P. B. (1999). Biological control of plant invaders: regional patterns, field experiments, and structured population models. Ecological Applications 9, 387–401.

Coudron, T. A. , Yocum, G. D. & Brandt, S. L. (2006). Nutrigenomics: a case study in the measurement of insect response to nutritional quality. Entomologia Experimentalis et Applicata 121, 1–14.

Croft, B. A. & Meyer, R. H. (1973). Carbamate and organophosphorus resistance patterns in populations of Amblyseius fallacis . Environmental Entomology 2, 691–696.

Cruaud, A. , Nidelet, S. , Arnal, P. , Weber, A. , Fusu, L. , Gumovsky, A. , Huber, J. , Polaszek, A. & Rasplus, J. Y. (2019). Optimized DNA extraction and library preparation for minute arthropods: application to target enrichment in chalcid wasps used for biocontrol. Molecular Ecology Resources 19, 702–710. PubMed

Davey, J. L. & Blaxter, M. W. (2010). RADseq: next‐generation population genetics. Briefings in Functional Genomics 9, 416–423. PubMed PMC

Dedeine, F. , Vavre, F. , Fleury, F. , Loppin, B. , Hochberg, M. E. & Bouletreau, M. (2001). Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proceedings of the National Academy of Sciences of the United States of America 98, 6247–6252. PubMed PMC

Dekkers, J. C. M. (2004). Commercial application of marker‐ and gene‐assisted selection in livestock: strategies and lessons. Journal of Animal Science 82(E‐Suppl), E313–E328. PubMed

Dennis, A. B. , Patel, V. , Oliver, K. M. & Vorburger, C. (2017). Parasitoid gene expression changes after adaptation to symbiont‐protected hosts. Evolution 71, 2599–2617. PubMed

Deplazes‐Zemp, A. , Abiven, S. , Schaber, P. , Schaepman, M. , Schaepman‐Strub, G. , Schmid, B. , Shimizu, K. K. & Altermatt, F. (2018). The Nagoya protocol could backfire on the global south. Nature Ecology and Evolution 2, 917–919. PubMed

Desjardins, C. A. , Perfectti, F. , Bartos, J. D. , Enders, L. S. & Werren, J. H. (2010). The genetic basis of interspecies host preference differences in the model parasitoid Nasonia . Heredity 104, 270–277. PubMed PMC

Dicke, M. , Cusumano, A. & Poelman, E. H. (2020). Microbial symbionts of parasitoids. Annual Review of Entomology 65, 171–190. PubMed

Drukker, B. , Janssen, A. , Willem, R. & Sabelis, M. W. (1997). Improved control capacity of the mite predator Phytoseiulus persimilis (Acari: Phytoseiidae) on tomato. Experimental & Applied Acarology 21, 507–518.

Dukas, R. (2000). Potential fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology 11, 536–543.

Dunham, W.C. (2015). Evolution and future of biocontrol. In 10th Annual Biocontrol Industry Meeting (ABIM), Basel, Switzerland.

Ekblom, R. & Wolf, J. B. W. W. (2014). A field guide to whole‐genome sequencing, assembly and annotation. Evolutionary Applications 7, 1026–1042. PubMed PMC

Facon, B. , Hufbauer, R. A. A. , Tayeh, A. , Loiseau, A. , Lombaert, E. , Vitalis, R. , Guillemaud, T. , Lundgren, J. G. G. & Estoup, A. (2011). Inbreeding depression is purged in the invasive insect Harmonia axyridis . Current Biology 21, 424–427. PubMed

Faino, L. & Thomma, B. P. H. J. (2014). Get your high‐quality low‐cost genome sequence. Trends in Plant Science 19, 288–291. PubMed

Falconer, D. S. & Mackay, T. F. C. (1996). Introduction to Quantitative Genetics. Longman, London.

Félix, M. A. & Barkoulas, M. (2015). Pervasive robustness in biological systems. Nature Reviews Genetics 16, 483–496. PubMed

Ferguson, K. B. (2020). Know your enemy: genomes of biological control agents PhD thesis, Wageningen University. 10.18174/511993. DOI

Ferguson, K.B. , Kursch‐Metz, T. , Verhulst, E.C & Pannebakker, B.A. (2020). Hybrid genome assembly and evidence‐based annotation of the egg parasitoid and biological control agent Trichogramma brassicae . G3: Genes|Genomes|Genetics. PubMed PMC

Floate, K. D. , Kyei‐Poku, G. K. & Coghlin, P. C. (2006). Overview and relevance of Wolbachia bacteria in biocontrol research. Biocontrol Science and Technology 16, 767–788.

Follett, P. A. , Duan, J. , Messing, R. H. & Jones, V. P. (2000). Parasitoid drift after biological control introductions: re‐examining Pandora's box. American Entomologist 46, 82–94.

Fouillet, P. , Bouletreau, M. , Vavre, F. , Fleury, F. & Varaldi, J. (2000). Evidence for female mortality in Wolbachia‐mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution 54, 191–200. PubMed

Gariepy, T. D. , Kuhlmann, U. , Gillott, C. & Erlandson, M. (2007). Parasitoids, predators and PCR: the use of diagnostic molecular markers in biological control of arthropods. Journal of Applied Entomology 131, 225–240.

Gariepy, T. D. , Kuhlmann, U. , Gillott, C. & Erlandson, M. (2008). A large‐scale comparison of conventional and molecular methods for the evaluation of host–parasitoid associations in non‐target risk‐assessment studies. Journal of Applied Ecology 45, 708–715.

Gariepy, V. , Boivin, G. & Brodeur, J. (2014). Why two species of parasitoids showed promise in the laboratory but failed to control the soybean aphid under field conditions. Biological Control 80, 1–7.

Geden, C. J. , Smith, L. , Long, S. J. & Rutz, D. A. (1992). Rapid deterioration of searching behavior, host destruction, and fecundity of the parasitoid Muscidifurax raptor (Hymenoptera: Pteromalidae) in culture. Annals of the Entomological Society of America 85, 179–187.

Geib, S. M. , Liang, G. H. , Murphy, T. D. & Sim, S. B. (2017). Whole genome sequencing of the braconid parasitoid wasp Fopius arisanus, an important biocontrol agent of pest tepritid fruit flies. G3 Genes|Genomes|Genetics 7, 2407–2411. PubMed PMC

Gomiero, T. , Pimentel, D. & Paoletti, M. G. (2011). Environmental impact of different agricultural management practices: conventional vs. organic agriculture. Critical Reviews in Plant Sciences 30, 95–154.

Goto, S. , Anbutsu, H. & Fukatsu, T. (2006). Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Applied and Environmental Microbiology 72, 4805–4810. PubMed PMC

Gotoh, T. , Noda, H. & Hong, X. Y. (2003). Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91, 208–216. PubMed

de Graaf, D. C. , Aerts, M. , Brunain, M. , Desjardins, C. A. , Jacobs, F. J. , Werren, J. H. & Devreese, B. (2010). Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic studies. Insect Molecular Biology 19, 11–26. PubMed PMC

Grau, T. , Vilcinskas, A. & Joop, G. (2017). Probiotic Enterococcus mundtii isolate protects the model insect Tribolium castaneum against Bacillus thuringiensis . Frontiers in Microbiology 8, 1261. PubMed PMC

Grbić, M. , van Leeuwen, T. , Clark, R. M. , Rombauts, S. , Rouzé, P. , Grbić, V. , Osborne, E. J. , Dermauw, W. , Thi Ngoc, P. C. , Ortego, F. , Hernández‐Crespo, P. , Diaz, I. , Martinez, M. , Navajas, M. , Sucena, É. , Magalhães, S. , Nagy, L. , Pace, R. M. , Djuranović, S. , Smagghe, G. , Iga, M. , Christiaens, O. , Veenstra, J. A. , Ewer, J. , Villalobos, R. M. , Hutter, J. L. , Hudson, S. D. , Velez, M. , Yi, S. V. , Zeng, J. , Pires‐daSilva, A. , Roch, F. , Cazaux, M. , Navarro, M. , Zhurov, V. , Acevedo, G. , Bjelica, A. , Fawcett, J. A. , Bonnet, E. , Martens, C. , Baele, G. , Wissler, L. , Sanchez‐Rodriguez, A. , Tirry, L. , Blais, C. , Demeestere, K. , Henz, S. R. , Gregory, T. R. , Mathieu, J. , Verdon, L. , Farinelli, L. , Schmutz, J. , Lindquist, E. , Feyereisen, R. & van de Peer, Y. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479, 487–492. PubMed PMC

Gross, M. (2013). EU ban puts spotlight on complex effects of neonicotinoids. Current Biology 23, R462–R464. PubMed

Gurung, K. , Wertheim, B. & Falcao Salles, J. (2019). The microbiome of pest insects: it is not just bacteria. Entomologia Experimentalis et Applicata 167, 156–170.

Handelsman, J. (2004). Metagenomics: application of genomics to uncultured microorganisms. Microbiology and Molecular Biology Reviews 68, 669–685. PubMed PMC

Hassan, S. A. (1994). Strategies to select Trichogramma species for use in biological control In Biological Control with Egg Parasitoids (eds Wajnberg E. and Hassan S.), pp. 55–71. CAB International, Wallingford.

Hassan, S. A. & Guo, M. F. (1991). Selection of effective strains of egg parasites of the genus Trichogramma (Hym., Trichogrammatidae) to control the European corn borer Ostrinia nubilalis Hb. (Lep., Pyralidae). Journal of Applied Entomology 111, 335–341.

Hayes, B. J. , Bowman, P. J. , Chamberlain, A. C. , Verbyla, K. & Goddard, M. E. (2009). Accuracy of genomic breeding values in multi‐breed dairy cattle populations. Genetics Selection Evolution 41, 51. PubMed PMC

Heimpel, G. E. & Mills, N. J. (2017). Biological Control: Ecology and Applications. Cambridge University Press, Cambridge.

Hein, S. , Poethke, H. J. & Dorn, S. (2009). What stops the ‘diploid male vortex’?‐a simulation study for species with single locus complementary sex determination. Ecological Modelling 220, 1663–1669.

Hertz‐Picciotto, I. , Sass, J. B. , Engel, S. , Bennett, D. H. , Bradman, A. , Eskenazi, B. , Lanphear, B. & Whyatt, R. (2018). Organophosphate exposures during pregnancy and child neurodevelopment: recommendations for essential policy reforms. PLoS Medicine 15, e1002671. PubMed PMC

Hoedjes, K. M. , Smid, H. M. , Vet, L. E. M. & Werren, J. H. (2014). Introgression study reveals two quantitative trait loci involved in interspecific variation in memory retention among Nasonia wasp species. Heredity 113, 542–550. PubMed PMC

Hoedjes, K. M. , Smid, H. M. , Schijlen, E. G. W. M. , Vet, L. E. M. & van Vugt, J. J. F. A. (2015). Learning‐induced gene expression in the heads of two Nasonia species that differ in long‐term memory formation. BMC Genomics 16, 162. PubMed PMC

Hoelmer, K. A. & Kirk, A. A. (2005). Selecting arthropod biological control agents against arthropod pests: can the science be improved to decrease the risk of releasing ineffective agents? Biological Control 34, 255–264.

Hohenlohe, P. A. , Hand, B. K. , Andrews, K. R. & Luikart, G. (2018). Population genomics provides key insights in ecology and evolution In Population Genomics (ed. Rajora O.), pp. 483–510. Springer, Cham.

Hoogendoorn, M. & Heimpel, G. E. (2001). PCR‐based gut content analysis of insect predators: using ribosomal ITS‐1 fragments from prey to estimate predation frequency. Molecular Ecology 10, 2059–2067. PubMed

Hopper, R. , Powell, W. , Roush, R. T. & Powell, W. (1993). Management of genetics of biological‐control introductions. The Annual Review of Entomology 38, 27–51.

Hoy, M. A. (1985). Improving establishment of arthropod natural enemies In Biological Control in Agriculture IPM Systems (eds Hoy M. and Herzo D.), pp. 155–166. Academic Press, New York.

Hoy, M. A. (1986). Use of genetic improvement in biological control. Agriculture, Ecosystems and Environment 15, 109–119.

Hsu, P. D. , Lander, E. S. & Zhang, F. (2014). Development and applications of CRISPR‐Cas9 for genome engineering. Cell 157, 1262–1278. PubMed PMC

Hudson, M. E. (2008). Sequencing breakthroughs for genomic ecology and evolutionary biology. Molecular Ecology Resources 8, 3–17. PubMed

Hufbauer, R. A. & Roderick, G. K. (2005). Microevolution in biological control: mechanisms, patterns, and processes. Biological Control 35, 227–239.

Hughes, G. L. , Rivero, A. & Rasgon, J. L. (2014). Wolbachia can enhance Plasmodium infection in mosquitoes: implications for malaria control? PLoS Pathogens 10, e1004182. PubMed PMC

Huigens, M. E. , Pashalidou, F. G. , Qian, M.‐H. , Bukovinszky, T. , Smid, H. M. , van Loon, J. J. A. , Dicke, M. & Fatouros, N. E. (2009). Hitch‐hiking parasitic wasp learns to exploit butterfly antiaphrodisiac. Proceedings of the National Academy of Sciences of the United States of America 106, 820–825. PubMed PMC

Hunt, E. J. , Loomans, A. J. M. & Kuhlmann, U. (2011). An international comparison of invertebrate biological control agent regulation: what can Europe learn? In Regulation of Biological Control Agents, pp. 79–112. Springer Netherlands, Dordrecht.

Jamin, A. R. & Vorburger, C. (2019). Estimating costs of aphid resistance to parasitoids conferred by a protective strain of the bacterial endosymbiont Regiella insecticola . Entomologia Experimentalis et Applicata 167, 252–260.

Janson, E. M. , Stireman, J. O. , Singer, M. S. & Abbot, P. (2008). Phytophagous insect‐microbe mutualisms and adaptive evolutionary diversification. Evolution 62, 997–1012. PubMed

Kamimura, Y. , Abe, J. , Ferreira, R. L. & Yoshizawa, K. (2019). Microsatellite markers developed using a next‐generation sequencing technique for Neotrogla spp. (Psocodea: Prionoglarididae), cave dwelling insects with sex‐reversed genitalia. Entomological Science 22, 48–55.

Kim, J. & Kim, J. S. (2016). Bypassing GMO regulations with CRISPR gene editing. Nature Biotechnology 34, 1014–1015. PubMed

Kondo, N. , Shimada, M. & Fukatsu, T. (2005). Infection density of Wolbachia endosymbiont affected by co‐infection and host genotype. Biology Letters 1, 488–491. PubMed PMC

Koskinioti, P. , Ras, E. , Augustinos, A. A. , Tsiamis, G. , Beukeboom, L. W. , Caceres, C. & Bourtzis, K. (2019). The effects of geographic origin and antibiotic treatment on the gut symbiotic communities of Bactrocera oleae populations. Entomologia Experimentalis et Applicata 167, 197–208.

Koskinioti, P. , Ras, E. , Augustinos, A. A. , Beukeboom, L. W. , Mathiopoulos, K. D. , Caceres, C. & Bourtzis, K. (2020a). Manipulation of insect gut microbiota towards the improvement of Bactrocera oleae artificial rearing. Entomologia Experimentalis et Applicata 168, 523–540.

Koskinioti, P. , Ras, E. , Augustinos, A. A. , Beukeboom, L. W. , Mathiopoulos, K. D. , Caceres, C. & Bourtzis, K. (2020b). The impact of fruit fly gut bacteria on the rearing of the parasitic wasp, Diachasmimorpha longicaudata . Entomologia Experimentalis et Applicata 168, 541–559.

Kraaijeveld, K. , Oostra, V. , Liefting, M. , Wertheim, B. , de Meijer, E. & Ellers, J. (2018). Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis . BMC Genomics 19, 892. PubMed PMC

Kraaijeveld, K. , Neleman, P. , Mariën, J. , de Meijer, E. & Ellers, J. (2019). Genomic resources for Goniozus legneri, Aleochara bilineata and Paykullia maculata, representing three independent origins of the parasitoid lifestyle in insects. G3 Genes|Genomes|Genetics 9, 987–991. PubMed PMC

Krehenwinkel, H. , Kennedy, S. , Pekár, S. & Gillespie, R. G. (2017). A cost‐efficient and simple protocol to enrich prey DNA from extractions of predatory arthropods for large‐scale gut content analysis by Illumina sequencing. Methods in Ecology and Evolution 8, 126–134.

Kremer, N. , Charif, D. , Henri, H. , Bataille, M. , Prévost, G. , Kraaijeveld, K. & Vavre, F. (2009). A new case of Wolbachia dependence in the genus Asobara: evidence for parthenogenesis induction in Asobara japonica . Heredity 103, 248–256. PubMed

Kruidhof, H. M. , Kostenko, O. , Smid, H. M. & Vet, L. E. M. (2019). Integrating parasitoid olfactory conditioning in augmentative biological control: potential impact, possibilities, and challenges. Frontiers in Ecology and Evolution 7, 84.

Kruitwagen, A. , Beukeboom, L. W. & Wertheim, B. (2018). Optimization of native biocontrol agents, with parasitoids of the invasive pest Drosophila suzukii as an example. Evolutionary Applications 11, 1473–1497. PubMed PMC

Lande, R. & Thompson, R. (1990). Efficiency of marker‐assisted selection in the improvement of quantitative traits. Genetics 124, 743–756. PubMed PMC

Lee, P. L. M. (2017). DNA amplification in the field: move over PCR, here comes LAMP. Molecular Ecology Resources 17, 138–141. PubMed

van Lenteren, J. C. , Bolckmans, K. , Köhl, J. , Ravensberg, W. J. & Urbaneja, A. (2018). Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63, 39–59.

Leung, K. , van de Zande, L. & Beukeboom, L. W. (2019). Life history traits of the whiting polyploid line of the non‐CSD parasitoid Nasonia vitripennis . Entomologia Experimentalis et Applicata 167, 655–669. PubMed PMC

Li, H.‐S. , Pan, C. , de Clercq, P. , Ślipiński, A. & Pang, H. (2016). Variation in life history traits and transcriptome associated with adaptation to diet shifts in the ladybird Cryptolaemus montrouzieri . BMC Genomics 17, 281. PubMed PMC

Lirakis, M. & Mägalhães, S. (2019). Does experimental evolution produce better biological control agents? Entomologia Experimentalis et Applicata 167, 584–597.

Lommen, S. T. E. , de Jong, P. W. & Pannebakker, B. A. (2017). It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control – a review. Entomologia Experimentalis et Applicata 162, 108–123.

Loomans, A. (2007). Regulation of invertebrate Biological Control Agents in Europe: review and recommendations in its pursuit of a harmonised regulatory system. Report EU project REBECA [Regulation of Biological Control Agents].

Lopes, M. S. , Bovenhuis, H. , Hidalgo, A. M. , van Arendonk, J. A. M. , Knol, E. F. & Bastiaansen, J. W. M. (2017). Genomic selection for crossbred performance accounting for breed‐specific effects. Genetics Selection Evolution 49, 51. PubMed PMC

Luan, T. , Woolliams, J. A. , Lien, S. , Kent, M. , Svendsen, M. & Meuwissen, T. H. E. (2009). The accuracy of genomic selection in Norwegian red cattle assessed by cross‐validation. Genetics 183, 1119–1126. PubMed PMC

Lynch, M. & Walsh, B. (1998). Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc, Sunderland.

Machtelinckx, T. , van Leeuwen, T. , Vanholme, B. , Gehesquière, B. , Dermauw, W. , Vandekerkhove, B. , Gheysen, G. & de Clercq, P. (2009). Wolbachia induces strong cytoplasmic incompatibility in the predatory bug Macrolophus pygmaeus . Insect Molecular Biology 18, 373–381. PubMed

Mackauer, M. (1976). Genetic problems in the production of biological control agents. Annual Review of Entomology 21, 369–385.

Malausa, J. C. , Blanchet, A. , Bon, M. C. , Cheyppe‐Buchmann, S. , Groussier‐Bout, G. , Jones, W. , Pickett, C. , Ris, N. , Roche, M. , Thaon, M. & Fauvergue, X. (2010). Introduction of the African parasitoid Psyttalia lounsburyi in south of France for the classical biological control of Bactrocera oleae . IOBC/WPRS Bulletin 59, 163–170.

Mallapaty, S. (2019). Australian gene‐editing rules adopt ‘middle ground’. Nature News https://www.nature.com/articles/d41586-019-01282-8 [accessed 22 October 2019]. PubMed

Mansur, L. M. , Lark, K. G. , Kross, H. & Oliveira, A. (1993). Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean (Glycine max L.). Theoretical and Applied Genetics 86, 907–913. PubMed

Mason, P. G. , Cock, M. J. W. , Barratt, B. I. P. , Klapwijk, J. N. , van Lenteren, J. C. , Brodeur, J. , Hoelmer, K. A. & Heimpel, G. E. (2018). Best practices for the use and exchange of invertebrate biological control genetic resources relevant for food and agriculture. BioControl 63, 149–154.

Meuwissen, T. H. , Hayes, B. J. & Goddard, M. E. (2001). Prediction of total genetic value using genome‐wide dense marker maps. Genetics 157, 1819–1829. PubMed PMC

Michalak, P. , Kang, L. , Schou, M. F. , Garner, H. R. & Loeschcke, V. (2019). Genomic signatures of experimental adaptive radiation in Drosophila . Molecular Ecology 28, 600–614. PubMed

Mills, N. J. & Kean, J. M. (2010). Behavioral studies, molecular approaches, and modeling: methodological contributions to biological control success. Biological Control 52, 255–262.

Miyatake, T. (1997). Genetic trade‐off between early fecundity and longevity in Bactrocera cucurbitae (Diptera: Tephritidae). Heredity 78, 93–100. PubMed

Mousseau, T. A. & Roff, D. A. (1987). Natural selection and the heritability of fitness components. Heredity 59, 181–197. PubMed

Narang, S. K. , Bartlett, A. C. & Faust, R. M. (1993). Applications of Genetics to Arthropods of Biological Control Significance. CRC Press, Boca Raton.

Nguyen, V. H. , Jonckheere, W. , Nguyen, D. T. , de Moraes, G. J. , van Leeuwen, T. & De Clerq, P. (2019). Phytoseiid mites prey effectively on thrips eggs: evidence from predation trials and molecular analyses. Biological Control 137, 104012.

Niehuis, O. , Gibson, J. D. , Rosenberg, M. S. , Pannebakker, B. A. , Koevoets, T. , Judson, A. K. , Desjardins, C. A. , Kennedy, K. , Duggan, D. , Beukeboom, L. W. , van De Zande, L. , Shuker, D. M. , Werren, J. H. , Gadau, J. , et al. (2010). Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia . PLoS One 5, e8597. PubMed PMC

Nishimura, O. , Brillada, C. , Yazawa, S. , Maffei, M. E. & Arimura, G. I. (2012). Transcriptome pyrosequencing of the parasitoid wasp Cotesia vestalis: genes involved in the antennal odorant‐sensory system. PLoS One 7, e50664. PubMed PMC

Nomikou, M. , Janssen, A. , Schraag, R. & Sabelis, M. W. (2001). Phytoseiid predators as potential biological control agents for Bemisia tabaci . Experimental and Applied Acarology 25, 271–291. PubMed

Nomikou, M. , Janssen, A. & Sabelis, M. W. (2003). Phytoseiid predators of whiteflies feed and reproduce on non‐prey food sources. Experimental and Applied Acarology 31, 15–26. PubMed

Nunney, L. (2003). Managing captive populations for release: a population‐genetic perspective In Quality Control and Production of Biological Control Agents: Theory and Testing Procedures (ed. van Lenteren J. C.), pp. 73–88. CABI International, Wallingford.

Oliver, K. M. , Moran, N. A. & Hunter, M. S. (2005). Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences of the United States of America 102, 12795–12800. PubMed PMC

Oliver, K. M. , Moran, N. A. & Hunter, M. S. (2006). Costs and benefits of a superinfection of facultative symbionts in aphids. Proceedings of the Royal Society B: Biological Sciences 273, 1273–1280. PubMed PMC

Oxley, P. R. , Spivak, M. & Oldroyd, B. P. (2010). Six quantitative trait loci influence task thresholds for hygienic behaviour in honeybees (Apis mellifera). Molecular Ecology 19, 1452–1461. PubMed

Page, R. E. , Fondrk, M. K. , Hunt, G. J. , Guzman‐Novoa, E. , Humphries, M. A. , Nguyen, K. & Greene, A. S. (2000). Genetic dissection of honeybee (Apis mellifera L.) foraging behavior. Journal of Heredity 91, 474–479. PubMed

Pannebakker, B. A. , Beukeboom, L. W. , Van Alphen, J. J. M. , Brakefield, P. M. & Zwaan, B. J. (2004). The genetic basis of male fertility in relation to haplodiploid reproduction in Leptopilina clavipes (Hymenoptera: Figitidae). Genetics 168, 341–349. PubMed PMC

Pannebakker, B. A. , Watt, R. , Knott, S. A. , West, S. A. & Shuker, D. M. (2011). The quantitative genetic basis of sex ratio variation in Nasonia vitripennis: a QTL study. Journal of Evolutionary Biology 24, 12–22. PubMed PMC

Pannebakker, B. A. , Trivedi, U. , Blaxter, M. A. , Watt, R. & Shuker, D. M. (2013). The transcriptomic basis of oviposition behaviour in the parasitoid wasp Nasonia vitripennis . PLoS One 8, e68608. PubMed PMC

Paolucci, S. , Salis, L. , Vermeulen, C. J. , Beukeboom, L. W. & van de Zande, L. (2016). QTL analysis of the photoperiodic response and clinal distribution of period alleles in Nasonia vitripennis . Molecular Ecology 25, 4805–4817. PubMed

Papanicolaou, A. , Schetelig, M. F. , Arensburger, P. , Atkinson, P. W. , Benoit, J. B. , Bourtzis, K. , Castañera, P. , Cavanaugh, J. P. , Chao, H. , Childers, C. , Curril, I. , Dinh, H. , Doddapaneni, H. V. , Dolan, A. , Dugan, S. , et al. (2017). The whole genome sequence of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), reveals insights into the biology and adaptive evolution of a highly invasive pest species. Genome Biology 18, 192. PubMed PMC

Paspati, A. , Ferguson, K. B. , Verhulst, E. C. , Urbaneja, A. , González‐Cabrera, J. & Pannebakker, B. A. (2019). Effect of mass rearing on the genetic diversity of the predatory mite Amblyseius swirskii Athias‐Henriot (Acari: Phytoseiidae). Entomologia Experimentalis et Applicata 167, 670–681.

Pizzol, J. , Pintureau, B. , Khoualdia, O. & Desneux, N. (2010). Temperature‐dependent differences in biological traits between two strains of Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). Journal of Pest Science 83, 447–452.

Plouvier, W. N. & Wajnberg, E. (2018). Improving the efficiency of augmentative biological control with arthropod natural enemies: a modeling approach. Biological Control 125, 121–130.

Poppy, G. M. & Powell, W. (2004). Genetic manipulation of natural enemies: can we improve biological control by manipulating the parasitoid and/or the plant? In Genetics, Evolution and Biological Control (eds Ehler T., Sforza L. E. and Mateille R.), pp. 219–233. CABI International, Wallingford.

Pratt, A. J. & MacRae, I. J. (2009). The RNA‐induced silencing complex: a versatile gene‐silencing machine. Journal of Biological Chemistry 284, 17897–17901. PubMed PMC

van der Putten, W. H. , Vet, L. E. M. , Harvey, J. A. & Wäckers, F. (2001). Linking above‐ and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends in Ecology & Evolution 16, 547–554.

Rahmani, H. , Hoffmann, D. , Walzer, A. & Schausberger, P. (2009). Adaptive learning in the foraging behavior of the predatory mite Phytoseiulus persimilis . Behavioral Ecology 20, 946–950.

Ram, A. & Sharma, A. K. (1977). Selective breeding for improving the fecundity and sex ratio of Trichogramma fasciatum (Perkins) (Trichogrammatidae: Hymenoptera), an egg parasite of lepidopterous hosts. Entomology 2, 133–137.

Ras, E. , Beukeboom, L. W. , Cáceres, C. & Bourtzis, K. (2017). Review of the role of gut microbiota in mass rearing of the olive fruit fly, Bactrocera oleae, and its parasitoids. Entomologia Experimentalis et Applicata 164, 237–256.

Rasmussen, L. B. , Jensen, K. , Sørensen, J. G. , Sverrisdóttir, E. , Nielsen, K. L. , Overgaard, J. , Holmstrup, M. & Kristensen, T. N. (2018). Are commercial stocks of biological control agents genetically depauperate? – A case study on the pirate bug Orius majusculus Reuter. Biological Control 127, 31–38.

Retamal, R. , Zaviezo, T. , Malausa, T. , Fauvergue, X. , Le Goff, I. & Toleubayev, K. (2016). Genetic analyses and occurrence of diploid males in field and laboratory populations of Mastrus ridens (Hymenoptera: Ichneumonidae), a parasitoid of the codling moth. Biological Control 101, 69–77.

Richards, S. & Murali, S. C. (2015). Best practices in insect genome sequencing: what works and what doesn't. Current Opinion in Insect Science 7, 1–7. PubMed PMC

Roderick, G. K. & Navajas, M. (2003). Genes in new environments: genetics and evolution in biological control. Nature Reviews Genetics 4, 889–899. PubMed

Rodriguez‐Saona, C. & Miller, J. C. (1995). Life history traits in Hippodamia convergens (Coleoptera: Coccinellidae) after selection for fast development. Biological Control 5, 389–396.

Roff, D. A. (2007). Contributions of genomics to life‐history theory. Nature Reviews Genetics 8, 116–125. PubMed

Rosenheim, J. A. & Hoy, M. A. (1988). Genetic improvement of a parasitoid biological control agent: artificial selection for insecticide resistance in Aphytis melinus (Hymenopera: Aphelinidae). Journal of Economic Entomology 81, 1539–1550.

Rossi, A. , Kontarakis, Z. , Gerri, C. , Nolte, H. , Hölper, S. , Krüger, M. & Stainier, D. Y. R. (2015). Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524, 230–233. PubMed

Rothacher, L. , Ferrer‐Suay, M. & Vorburger, C. (2016). Bacterial endosymbionts protect aphids in the field and alter parasitoid community composition. Ecology 97, 1712–1723. PubMed

Rougerie, R. , Smith, M. A. , Fernandez‐Triana, J. , Lopez‐Vaamonde, C. , Ratnasingham, S. & Hebert, P. D. N. (2011). Molecular analysis of parasitoid linkages (MAPL): gut contents of adult parasitoid wasps reveal larval host. Molecular Ecology 20, 179–186. PubMed

Rousch, R. (1990). Genetic variation in natural enemies: critical issues for colonization in biological control In Critical Issues in Biological Control (eds Mackauer M., Ehler L. E. and Roland J.), pp. 563–588. Intercept, Andover.

Roush, R. T. & Daly, J. C. (1990). The role of population genetics in resistance research and management In Pesticide Resistance in Arthropods (eds Roush R. T. and Tabashnik B. E.), pp. 97–152. Springer, Boston.

Roush, R. & Hoy, M. (1980). Selection improves Sevin resistance in spider mite predator. California Agriculture 34, 11–14.

Roush, R. T. & Hoy, M. A. (1981a). Genetic improvement of Metaseiulus occidentalis: selection with methomyl, dimethoate, and carbaryl and genetic analysis of carbaryl resistance. Journal of Economic Entomology 74, 138–141.

Roush, R. T. & Hoy, M. A. (1981b). Laboratory, glasshouse, and field studies of artificially selected carbaryl resistance in Metaseiulus occidentalis . Journal of Economic Entomology 74, 142–147.

Routray, S. , Dey, D. , Baral, S. , Das, A. P. & Mahantheshwara, B. (2016). Genetic improvement of natural enemies: a review. Agricultural Reviews 37, 325–332.

Rugman‐Jones, P. F. & Stouthamer, R. (2017). High‐resolution melt analysis without DNA extraction affords rapid genotype resolution and species identification. Molecular Ecology Resources 17, 598–607. PubMed

Russell, J. E. & Stouthamer, R. (2011). The genetics and evolution of obligate reproductive parasitism in Trichogramma pretiosum infected with parthenogenesis‐inducing Wolbachia . Heredity 106, 58–67. PubMed PMC

Sánchez‐Rosario, M. , Pérez‐Staples, D. , Toledo, J. , Valle‐Mora, J. & Liedo, P. (2017). Artificial selection on mating competitiveness of Anastrepha ludens for sterile insect technique application. Entomologia Experimentalis et Applicata 162, 133–147.

Schausberger, P. , Walzer, A. , Hoffmann, D. , Rahmani, H. , Behaviour, S. , June, N. , Schausberger, P. , Walzer, A. , Hoffmann, D. & Rahmani, H. (2010). Food imprinting revisited: early learning in foraging predatory mites. Behaviour 147, 883–897.

Schidlo, N. , Pannebakker, B. , Zwaan, B. , Beukeboom, L. & van Alphen, J. (2002). Curing thelytoky in the Drosophila parasitoid Leptopilina clavipes (Hymenoptera: Figitidae). Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 13, 93–96.

Schlötterer, C. , Tobler, R. , Kofler, R. & Nolte, V. (2014). Sequencing pools of individuals individuals—mining genome‐wide polymorphism data without big funding. Nature Reviews Genetics 15, 749–763. PubMed

Schmid, M. , Sieber, R. , Zimmermann, Y. S. & Vorburger, C. (2012). Development, specificity and sublethal effects of symbiont‐conferred resistance to parasitoids in aphids. Functional Ecology 26, 207–215.

Schuler, H. , Bertheau, C. , Egan, S. P. , Feder, J. L. , Riegler, M. , Schlick‐Steiner, B. C. , Steiner, F. M. , Johannesen, J. , Kern, P. , Tuba, K. , Lakatos, F. , Köppler, K. , Arthofer, W. & Stauffer, C. (2013). Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Molecular Ecology 22, 4101–4111. PubMed

Sørensen, J. G. , Addison, M. F. & Terblanche, J. S. (2012). Mass‐rearing of insects for pest management: challenges, synergies and advances from evolutionary physiology. Crop Protection 38, 87–94.

Spollen, K. M. & Hoy, M. A. (1992). Genetic improvement of an arthropod natural enemy: relative fitness of a carbaryl‐resistant strain of the California red scale parasite Aphytis melinus DeBach. Biological Control 2, 87–94.

Stahl, J. M. , Gariepy, T. D. , Beukeboom, L. W. & Haye, T. (2019). A molecular tool to identify Anastatus parasitoids of the brown marmorated stink bug. Entomologia Experimentalis et Applicata 167, 692–700.

Starý, P. (1999). Biology and distribution of microbe‐associated thelytokous populations of aphid parasitoids (Hym., Braconidae, Aphidiinae). Journal of Applied Entomology 123, 231–236.

Stearns, S. C. (1989). Trade‐offs in life‐history evolution. Functional Ecology 3, 259–268.

Stiling, P. & Cornelissen, T. (2005). What makes a successful biocontrol agent? A meta‐analysis of biological control agent performance. Biological Control 34, 236–246.

Stokstad, E. (2018). European agency concludes controversial ‘neonic’ pesticides threaten bees. Science Magazine https://www.sciencemag.org/news/2018/02/european-agency-concludes-controversial-neonic-pesticides-threaten-bees [accessed 21 October 2019].

Stouthamer, R. & Kazmer, D. J. (1994). Cytogenetics of microbe‐associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73, 317–327.

Stouthamer, R. & Nunney, L. (2014). Can neutral molecular markers be used to determine the success of an introduction of a “better” strain into an established population of a biocontrol parasitoid? Journal of Economic Entomology 107, 483–495. PubMed

Stouthamer, R. , Luck, R. F. & Hamilton, W. D. (1990). Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex. Proceedings of the National Academy of Sciences of the United States of America 87, 2424–2427. PubMed PMC

Stouthamer, R. , Luck, R. F. & Werren, J. H. (1992). Genetics of sex determination and the improvement of biological control using parasitoids. Environmental Entomology 21, 427–435.

Stouthamer, R. , Hu, J. , van Kan, F. J. P. M. , Platner, G. R. & Pinto, J. D. (1999). The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma . BioControl 43, 421–440.

Sumer, F. , Tuncbilek, A. S. , Oztemiz, S. , Pintureau, B. , Rugman‐Jones, P. & Stouthamer, R. (2009). A molecular key to the common species of Trichogramma of the Mediterranean region. BioControl 54, 617–624.

Supple, M. A. & Shapiro, B. (2018). Conservation of biodiversity in the genomics era. Genome Biology 19, 131. PubMed PMC

Szűcs, M. , Salerno, P. E. , Teller, B. J. , Schaffner, U. , Littlefield, J. L. & Hufbauer, R. A. (2019). The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations. Evolutionary Applications 12, 470–481. PubMed PMC

Tang, L. D. , Wang, X. M. , Jin, F. L. , Qiu, B. L. , Wu, J. H. & Ren, S. X. (2014). De novo sequencing‐based transcriptome and digital gene expression analysis reveals insecticide resistance‐relevant genes in Propylaea japonica (Thunberg) (Coleoptea: Coccinellidae). PLoS One 9, e100946. PubMed PMC

Tautz, D. , Ellegren, H. & Weigel, D. (2010). Next generation molecular ecology. Molecular Ecology 19, 1–3. PubMed

Thomas, M. B. & Willis, A. J. (1998). Biocontrol ‐ risky but necessary? Trends in Ecology and Evolution 13, 325–329. PubMed

Thomas, A. P. , Trotman, J. , Wheatley, A. , Aebi, A. , Zindel, R. & Brown, P. M. J. (2013). Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR‐based gut analysis. Insect Conservation and Diversity 6, 20–27.

Thrall, P. H. , Oakeshott, J. G. , Fitt, G. , Southerton, S. , Burdon, J. J. , Sheppard, A. , Russell, R. J. , Zalucki, M. , Heino, M. & Ford Denison, R. (2011). Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro‐ecosystems. Evolutionary Applications 4, 200–215. PubMed PMC

Turlings, T. C. J. & Wäckers, F. (2004). Recruitment of predators and parasitoids by herbivore‐injured plants. Advances in Insect Chemical Ecology 2, 21–75.

VanRaden, P. M. , van Tassell, C. P. , Wiggans, G. R. , Sonstegard, T. S. , Schnabel, R. D. , Taylor, J. F. & Schenkel, F. S. (2009). Invited review: reliability of genomic predictions for north American Holstein bulls. Journal of Dairy Science 92, 16–24. PubMed

Vavre, F. , Fouillet, P. & Fluery, F. (2003). Between‐ and within‐host species selection on cytoplasmic incompatibility‐inducing Wolbachia in haploidiploids. Evolution 57, 421–427. PubMed

Veneti, Z. , Zabalou, S. , Papafotiou, G. , Paraskevopoulos, C. , Pattas, S. , Livadaras, I. , Markakis, G. , Herren, J. K. , Jaenike, J. & Bourtzis, K. (2012). Loss of reproductive parasitism following transfer of male‐killing Wolbachia to Drosophila melanogaster and Drosophila simulans . Heredity 109, 306–312. PubMed PMC

Verhulst, E. C. , Beukeboom, L. W. & van de Zande, L. (2010). Maternal control of haplodiploid sex determination in the wasp Nasonia . Science 328, 620–623. PubMed

Voroshilov, N. V. (1979). Breeding of thermoresistant lines of Phytoseiulus (Phytoseiulus persimilis AH). Genetika 15, 70–76.

Wajnberg, E. (2004). Measuring genetic variation in natural enemies used for biological control: why and how? In Genetics, Evolution and Biological Control (eds Ehler T., Sforza L. E. and Mateille R.), pp. 19–37. CABI International, Wallingford.

Wajnberg, E. , Bernstein, C. & van Alphen, J. (2008). Behavioral Ecology of Insect Parasitoids: From Theoretical Approaches to Field Applications. Blackwell Publishing Ltd, Oxford.

Wajnberg, E. , Roitberg, B. D. & Boivin, G. (2016). Using optimality models to improve the efficacy of parasitoids in biological control programmes. Entomologia Experimentalis et Applicata 158, 2–16.

Waltz, E. (2016). Gene‐edited CRISPR mushroom escapes US regulation. Nature 532, 293. PubMed

Wang, Z. , Mark, G. , Snyder, M. , Gerstein, M. & Snyder, M. (2009). RNA‐Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 10, 57–63. PubMed PMC

Wang, X. , Werren, J. H. & Clark, A. G. (2015). Genetic and epigenetic architecture of sex‐biased expression in the jewel wasps Nasonia vitripennis and giraulti . Proceedings of the National Academy of Sciences of the United States of America 112, E3545–E3554. PubMed PMC

Werren, J. H. , Baldo, L. & Clark, M. E. (2008). Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741–751. PubMed

Werren, J. H. , Richards, S. , Desjardins, C. A. , Niehuis, O. , Gadau, J. , Colbourne, J. K. & The Nasonia Genome Working Group (2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327, 343–348. PubMed PMC

Wetterstrand, K.A. (2019). DNA Sequencing Costs: Data from the NHGRI Genome Sequencing Program (GSP). https://www.genome.gov/about-genomics/fact-sheets/DNA-Sequencing-Costs-Data [accessed 10 May 2019].

White, E. B. , Debach, P. & Garber, M. J. (1970). Artificial selection for genetic adaptation to temperature extremes in Aphytis linganensis compere (Hymenoptera: Aphelinidae). Hilgardia 40, 161–192.

Willer H. & Lernoud J. (eds) (2019). The World of Organic Agriculture. Statistics and Emerging Trends 2019. Research Institute of Organic Agriculture (FiBL), Frick, and IFOAM—Organics International, Bonn.

Williams, G. C. (1996). Adaptation and Natural Selection: A Critique of some Current Evolutionary Thought. Princeton University Press, Princeton.

Woodworth, L. M. , Montgomery, M. E. , Briscoe, D. A. & Frankham, R. (2002). Rapid genetic deterioration in captive populations: causes and conservation implications. Conservation Genetics 3, 277–288.

Xia, S. (2020). Exploring the potential of genetic improvement of insects: A case study using the haplodiploid parasitoid wasp Nasonia vitripennis. PhD thesis, Wageningen University. doi: 10.18174/518107 DOI

Xia, S. , Pannebakker, B. A. , Groenen, M. A. M. , Zwaan, B. J. & Bijma, P. (2020). Quantitative genetics of wing morphology in the parasitoid wasp Nasonia vitripennis: hosts increase sibling similarity. Heredity 125, 40–49. PubMed PMC

Yamashita, S. & Takahashi, K. H. (2018). Artificial transfer of a thelytoky‐inducing Wolbachia endosymbiont between strains of the endoparasitoid wasp Asobara japonica (Hymenoptera: Braconidae). Applied Entomology and Zoology 53, 403–409.

Ye, Y. H. , Seleznev, A. , Flores, H. A. , Woolfit, M. & McGraw, E. A. (2017). Gut microbiota in Drosophila melanogaster interacts with Wolbachia but does not contribute to Wolbachia‐mediated antiviral protection. Journal of Invertebrate Pathology 143, 18–25. PubMed

Yocum, G. D. , Coudron, T. A. & Brandt, S. L. (2006). Differential gene expression in Perillus bioculatus nymphs fed a suboptimal artificial diet. Journal of Insect Physiology 52, 586–592. PubMed

Zaviezo, T. , Retamal, R. , Urvois, T. , Fauvergue, X. , Blin, A. & Malausa, T. (2018). Effects of inbreeding on a gregarious parasitoid wasp with complementary sex determination. Evolutionary Applications 11, 243–253. PubMed PMC

Zayed, A. & Packer, L. (2005). Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proceedings of the National Academy of Sciences of the United States of America 102, 10742–10746. PubMed PMC

Zhang, G. , Li, Y. , Tian, C. , Xu, Y. , Zhou, H. , Huang, J. , Wang, J. & Liu, H. (2018). Intraspecific variations on thermal susceptibility in the predatory mite Neoseiulus barkeri Hughes (Acari: Phytoseiidae): responding to long‐term heat acclimations and frequent heat hardenings. Biological Control 121, 208–215.

Zhao, Y. , Wang, F. , Zhang, X. , Zhang, S. , Guo, S. , Zhu, G. , Liu, Q. & Li, M. (2016). Transcriptome and expression patterns of chemosensory genes in antennae of the parasitoid wasp Chouioia cunea . PLoS One 11, e0148159. PubMed PMC

Jekyll or Hyde? The genome (and more) of Nesidiocoris tenuis, a zoophytophagous predatory bug that is both a biological control agent and a pest