Abstract

Genetics has long played a role in the history of insect pest management, Beginning from simple collections of mutations and the development of chromosome linkage maps, many of the early applications of genetic technology were focused on the development of new strains for the sterile insect technique as a form of biological control. Since that time, and as the field of genetics underwent a true merger with molecular biology, the focus shifted almost entirely to methods using molecular technology. These methods had the advantage of being more broadly applicable to control of a wide range of pest species, from the frustrations often associated with attempts to transfer genetic tools developed in Drosophila directly to these species. The latest applications of molecular genetic technologies in the area of genetically based control methods now also include cutting-edge systems for genome editing and the use of RNA inhibition for selectively knocking out the expression of individual genes. Finally, as the field of genetics has shifted its focus from the analysis of individual genes to that of entire genomes, We outline some policy considerations for taking genetic insect control systems through to field implementation.

• 1.   Dale J, Schantz M, Plant N. From genes to genomes: concepts and applications of DNA technology. 3rd ed. West Sussex (UK): John Wiley and Sons; 2012.
• 2.   Gould S. The panda’s thumb. New York: W.W. Norton and Company; 1980.
• 3.   Atkinson PW. Genetic engineering in insects of agricultural importance. Insect Biochem Mol Biol. 2002;32:1237–43.
• 4.   James A. Control of disease transmission through genetic modification of mosquitoes. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 319–33.
• 5.   Robinson A. Mutations and their use in insect control. Mutat Res. 2002;511:113–32.
• 6.   Boëtel C, Beisel U, Castro L, Césard N, Reeves R. Engaging scientists: an online survey exploring the experience of innovative biotechnological approaches to controlling vector borne diseases. Parasit Vectors. 2015;8:414.
• 7.   Stratikopoulos EE, Augustinos AA, Petalas GY, Vrahatis MN, Mintzas A, Mathiopoulos KD, et al. An integrated genetic and cytogenetic map for the Mediterranean fruit fly, Ceratitis capitata, based on microsatellite and morphological markers. Genetica. 2008;133(2):147–57.
• 8.   Roethele J, Romero-Sevenson J, Feder J. Evidence for broad-scale conservation of linkage map relationships between Rhagoletis pomonella (Diptera: Tephritidae) and Drosophila melanogaster (Diptera: Drosophilidae). Ann Entomol Soc Am. 2001;94:936–47.
• 9.   Lindsley D, Grell E. Genetic variations of Drosophila melanogaster. Washington: Carnegie Institute of Washington; 1968. Publication No.: 627.
• 10.   Childress D. Polytene chromosomes and linkage group-chromosome correlations in the Australian sheep blowfly Lucillia cuprina (Diptera: Calliphoridae). Chromosoma. 1969;26:208–14.
• 11.   Foster GG, Whitten MJ, Konovalov C, Bedo DG, Maddern RH, Boon DT. Cytogenetic studies of Lucillia cuprina dorsalis R.D. (Diptera: Calliphoridae). Polytene chromosome maps of the autosomes and cytogenetic localization of visible genetic markers. Chromosoma. 1980;81:151–68.
• 12.   Garcia-Martinez V, Hernandez-Ortiz E, Zepeta-Cisneros CS, Robinson AS, Zacharopoulou A, Franz G. Mitotic and polytene chromosome analysis in the Mexican fruit fly, Anastrepha ludens (Loew) (Diptera: Tephritidae). Genome. 2009;52:20–30.
• 13.   Ashburner M. Drosophila: a laboratory handbook. Cold Spring Harbor (NY): Cold Spring Harbor Press; 1989.
• 14.   Hoy M. Insect molecular genetics. Waltham (MA): Academic Press; 2013.
• 15.   Haymer D. Random amplified polymorphic DNAs and microsatellites: what are they, and can they tell us anything we don’t already know? Ann Entomol Soc Am. 1994;87(6):717–22.
• 16.   Bonizzoni M, Malacrida AR, Guglielmino CR, Gomulski LM, Gasperi G, Zheng L. Microsatellite polymorphism in the Mediterranean fruit fly Ceratitis capitata. Insect Mol Biol. 2000;9:251–9.
• 17.   Drosopoulou E, Koeppler K, Kounatidis I, Nakou I, Papadopoulos N, Bourtzis K, et al. Genetic and cytogenetic analysis of the walnuthusk fly (Diptera: Tephritidae). Ann Entomol Soc Am. 2010;103(6):1003–11.
• 18.   Hawthorne D. AFLP-based genetic linkage map of the Colorado potato beetle Leptinotarsa decemlineata: sex chromosomes and a pyrethroid-resistance candidate gene. Genetics. 2001;158:695–700.
• 19.   Hunt G, Page R. Linkage map of the honey bee, Apis mellifera, based on RAPD markers. Genetics. 1995;139:1371–82.
• 20.   Homchan S, Haymer D, Kitthawee S. Microsatellite marker variation in populations of the melon fly parasitoid, Psyttalia fletcheri. ScienceAsia. 2014;40:348–54.
• 21.   Klassen W, Curtis C. History of the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A, editors. Sterile insect technique. Dordrecht (Netherlands): Springer; 2005. p. 3–36.
• 22.   Klassen W. Area-wide integrated pest management and the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A, editors. Sterile insect technique. Dordrecht (Netherlands): Springer; 2005. p. 39–68.
• 23.   Robinson A, Hendrichs J. Prospects for the future development and application of the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A, editors. Sterile insect technique. Dordrecht (Netherlands): Springer; 2005. p. 728–86.
• 24.   Knipling E. Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol. 1955;48:459–62.
• 25.   Robinson A. Genetic sexing strains in medfly, Ceratitis capitata, sterile insect technique programmes. Genetica. 2002;116:5–13.
• 26.   Lifschitz E, Cladera J. Ceratitis capitata: cytogenetics and sex determination. In: Robinson AS, Hooper G, editors. Fruit flies: their biology, natural enemies and control. New York: Elsevier; 1989. p. 3-11.
• 27.   Anleitner J, Haymer D. Y enriched and Y specific DNA sequences from the genome of the Mediterranean fruit fly, Ceratitis capitata. Chromosoma. 1992;101:271–8.
• 28.   Douglas L, Untalan P, Haymer D. Molecular sexing in the Mediterranean fruit fly, Ceratitis capitata. Insect Biochem Mol Biol. 2004;34:159–65.
• 29.   Franz G, Robinson A. Molecular technologies to improve the effectiveness of the sterile insect technique. Genetica. 2011;139:1–5.
• 30.   McInnis D, Tam S, Lim R, Komatsu J, Kurashima R, Albrecht C. Development of a pupal color-based genetic sexing strain of the melon fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Ann Entomol Soc Am. 2004;97(5):1026–33.
• 31.   Alphey L, Andreasen M. Dominant lethality and insect population control. Mol Biochem Parasitol. 2002;121:173–8.
• 32.   Franz G. Genetic sexing strains in Mediterranean fruit fly, and example for other species amenable to large scale rearing for the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A, editors. Sterile insect technique. Dordrecht (Netherlands): Springer; 2005. p. 427–51.
• 33.   Handler A. An introduction to the history and methodology of insect gene transfer. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 3–26.
• 34.   Robinson A, Franz G, Atkinson P. Insect transgenesis and its potential role in agriculture and human health. Insect Biochem Mol Biol. 2004;34:113–20.
• 35.   McInnis D, Haymer D, Tam S, Thanaphum S. Ceratitis capitata (Diptera: Tephritidae): transient expression of a heterologous gene for resistance to the antibiotic geneticin. Ann Entomol Soc Am. 1990;83(5):982–6.
• 36.   Handler A. Understanding and improving transgene stability and expression in insects for SIT and conditional lethal release programs. Insect Biochem Mol Biol. 2004;34:121–30.
• 37.   Ashburner M. Medfly transformed-Official! Science. 1995;270:1941–2.
• 38.   Beverley S, Wilson A. Molecular evolution in Drosophila and the higher Diptera. J Mol Evol. 1984;21:1–13.
• 39.   Pavlopoulos A, Oehler S, Kapetanaki M, Savakis C. The DNA transposon Minos as a tool for transgenesis and functional genomic analysis in vertebrates and invertebrates. Genome Biol. 2007;8 Suppl 1:S2.
• 40.   Lampe D, Waldon K, Sherwood J, Robertson H. Genetic engineering of insects with mariner transposons. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 237–48.
• 41.   Atkinson P, O’Brochta D. Hermes and other hAT elements as gene vectors in insects. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 219–36.
• 42.   Sagri E, Reczko M, Tsoumani K, Gregoriou M, Harokopos V, Mavridou A, et al. The molecular biology of the olive fly comes of age. BMC Genet. 2014;15 Suppl 2:58.
• 43.   Fraser M. The TTAA-specific family of transposable elements. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 249–68.
• 44.   Handler AM. Use of the piggyBac transposon for germ-line transformation of insects. Insect Biochem Mol Biol. 2002;32(10):1211–20.
• 45.   Hoy M. Deploying transgenic arthropods in pest management programs: risks and realities. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 335–79.
• 46.   Saccone G, Salvemini M, Polito L. The transformer gene of Ceratitis capitata: a paradigm for a conserved epigenetic master regulator of sex determination in insects. Genetica. 2011;139:99–111.
• 47.   He M, Haymer D. Codon bias in actin multigene families and effects on the reconstruction of phylogenetic relationships. J Mol Evol. 1995;41:141–9.
• 48.   Shearman D, Fromme M. The Bactrocera tryoni homologue of the Drosophila melanogaster sex-determination gene doublesex. Insect Mol Biol. 1998;7(4):355–66.
• 49.   Kuhn S, Sievert V, Traut W. The sex-determining gene doublesex in the fly Megaselia scalaris: conserved structure and sex-specific splicing. Genome. 2000;43(6):1011–20.
• 50.   Scali C, Catteruccia F, Li Q, Crisanti A. Identification of sex-specific transcripts of the Anopheles gambiae doublesex gene. J Exp Biol. 2005;208:3701–9.
• 51.   Wilhoeft U, Franz G. Identification of the sex-determining region of the Ceratitis capitata Y chromosome by deletion mapping. Genetics. 1996;144:737–45.
• 52.   Zhou Q, Untalan P, Haymer D. Repetitive A–T rich DNA sequences from the Y chromosome of the Mediterranean fruit fly Ceratitis capitata. Genome. 2000;43:434–8.
• 53.   Young O, Ingebritsen S, Foudin A. Regulation of transgenic arthropods and other invertebrates in the United States. In: Handler A, James A, editors. Insect transgenesis. Boca Raton (FL): CRC Press; 2000. p. 369–79.
• 54.   Hsu P, Lander E, Zhang F. Development and applications of CRISPR–Cas9 for genome engineering. Cell. 2014;157:1262–78.
• 55.   Sander J, Joung J. CRISPR–CAS systems for editing, regulating and targeting genomes. Nat Biotechnol. 2014;32:347–55.
• 56.   Bassett A, Liu JL. CRISPR–Cas9 and genome editing in Drosophila. J Genet Genomics. 2014;41:7–19.
• 57.   Schmitt-Engel C, et al. The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology. Nat Commun. 2014;6:8822.
• 58.   Hsu JC, Chien TY, Hu CC, Chen J, Wu WJ, Feng HT, et al. Discovery of genes related to insecticide resistance in Bactrocera dorsalis by functional genomic analysis of a de novo assembled transcriptome. PLoS One. 2012;7(8):e40950.
• 59.   Schetelig M, Caceres C, Zacharopoulou A, Franz G, Wimmer E. Conditional embryonic lethality to improve the sterile insect technique in Ceratitis capitata (Diptera: Tephritidae). BMC Biol. 2009;7:4.
• 60.   Tabashnik BE, Gassmann AJ, Crowder DW, Carriere Y. Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol. 2008;26:199–202.
• 61.   Tabashnik BE, Brevault T, Carriere Y. Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol. 2013;31:510–21.
• 62.   Tan A, Fu G, Jin L, et al. Transgene based, female specific lethality system for genetic sexing of the silkworm, Bombyx mori. Proc Natl Acad Sci U S A. 2013;110:6766–70.
• 63.   Thomas DD, Donnelly CA, Wood RJ, Alphey LS. Insect population control using a dominant, repressible, lethal genetic system. Science. 2000;287:2474–6.
• 64.   Thompson S. Density dependence of controlling insect populations [MSc thesis]. London: Imperial College London; 2015.
• 65.   Vargas Teran M, Hofmann HC, Tweddle NE. Impact of screwworm eradication programmes using the sterile insect technique. In: Dyck V, Hendrichs J, Robinson A, editors. Sterile insect technique: principles and practice in area-wide integrated pest management. Dordrecht (Netherlands): Springer; 2005. p. 629–50.
• 66.   Watkinson Powell B, Alphey N. Resistance to genetic insect control: modelling the effects of space. J Theor Biol. 2017;413:72–85.
• 67.   Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008;6:741–51.
• 68.   WHO/TDR, FNIH. The guidance framework for testing genetically modified mosquitoes. Geneva: World Health Organization; 2014.
• 69.   Wise de Valdez MR, Nimmo D, Betz J, Gong HF, James AA, Alphey L, Black WC 4th. Genetic elimination of dengue vector mosquitoes. Proc Natl Acad Sci U S A. 2011;108:4772–5.
• 70.   Yakob L, Alphey L, Bonsall MB. Aedes aegypti control: the concomitant role of competition, space and transgenic technologies. J Appl Ecol. 2008;45:1258–65.
• 71.   Zalucki MP, Shabbir A, Silva R, Adamson D, Shu Sheng L, Furlong MJ. Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? J Econ Entomol. 2012;105:1115–29.

Data Sharing Statement

Funding