遗传不育技术在蚊媒疾病防控中的应用
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  • 英文篇名:Application of genetic pest management in the control of mosquito-borne diseases
  • 作者:王玉生 ; 李建伟 ; 张桂芬 ; 严盈 ; 李昕玥 ; 万方浩
  • 英文作者:Yu-sheng WANG;Jian-wei LI;Gui-fen ZHANG;Ying YAN;Xin-yue LI;Fang-hao WAN;State Key Laboratory for Biology of Plant Diseases and Insect Pests,Institute of Plant Protection,Chinese Academy of Agricultural Sciences;Department of Entomology,North Carolina State University;Genetic Engineering and Society Center and W. M. Keck Center for Behavioral Biology,North Carolina State University;College of Agriculture and Plant Protection,Qingdao Agricultural University;
  • 关键词:蚊媒昆虫 ; 遗传防治 ; 昆虫不育技术 ; 释放携带显性致死基因昆虫的技术
  • 英文关键词:disease vector mosquito;;genetic control;;sterile insect technique;;release of insects carrying a dominant lethal
  • 中文刊名:HDKC
  • 英文刊名:Journal of Biosafety
  • 机构:中国农业科学院植物保护研究所,植物病虫害生物学国家重点实验室;Department of Entomology,North Carolina State University;Genetic Engineering and Society Center and W. M. Keck Center for Behavioral Biology,North Carolina State University;青岛农业大学农学与植物保护学院;
  • 出版日期:2015-05-15
  • 出版单位:生物安全学报
  • 年:2015
  • 期:v.24
  • 基金:国家“973”计划项目(2009CB119200);; 国家“十一五”科技支撑计划课题(2006BAD08A18);; 农业部农作物病虫害疫情监测与防治项目(2003-2015);; 中国农科院科技创新工程(2013-2015);; 人力资源社会保障部2014年度留学人员科技活动择优资助项目
  • 语种:中文;
  • 页:HDKC201502010
  • 页数:13
  • CN:02
  • ISSN:35-1307/Q
  • 分类号:78-90
摘要
疟疾、登革热等重大传染性蚊媒疾病严重危害人类健康,且目前缺乏有效的药物和疫苗,防治埃及伊蚊、冈比亚按蚊等媒介昆虫是控制和消除这些疾病的有效手段。化学杀虫剂的大规模使用在一定程度上控制了疾病的传播,但其抗药性和环境污染等问题也随之而来。分子生物学的飞速发展为昆虫不育技术(SIT)的更新及害虫防治提供了新的策略,由此发展起来的以释放携带显性致死基因昆虫(RIDL)为代表的一系列遗传不育技术为蚊虫种群防控提供了更加有效的选择。本文概述了遗传技术在蚊虫防控中的应用进展,包括蚊虫遗传防治的历史和策略,阐述了RIDL技术体系的原理,同时介绍了相关遗传控制品系和已经开展的田间释放研究,展示了遗传修饰不育技术在蚊媒疾病防治中的巨大潜力。
        Mosquito-borne diseases,such as dengue fever and malaria,are global problems and pose a serious threat to public health. An estimated 2. 5 billion people live in areas at the risk of epidemic transmission. For now,no vaccines are available against the pathogens respnsible for these diseases,and the mosquito control is considered as one of the most effective ways to reduce transmission. Mass application of pesticides could reduce the mosquito population but it also brings problems like insect resistance and environmental pollution. The release of insects with dominant lethality( RIDL) technology and other genetic control systems based on the traditional sterile insect technique( SIT) provide new strategies to control disease vector mosquitos,such as Aedes aegypti and Anopheles gambiae. Those new version of genetic control methods are species-specific and environment-friendly,and now being developed and tested worldwide. Here the principle and recent progress of mosquito genetic control are reviewed. The history of mosquito SIT is introduced,and the genetic control strategies including self-limiting and self-sustaining populations are also illustrated.The development,as well as laboratory and field trials of RIDL strains are described. It is suggested that genetic control strategies such as RIDL are promising methods to fight against mosquitoes carrying human diseases.
引文
Alphey L.2014.Genetic control of mosquitoes.Annual Reviewof Entomology,59:205-224.
    Alphey L,Benedict M,Bellini R,Clark G G,Dame D A,Service M W and Dobson S L.2010.Sterile-insect methodsfor control of mosquito-borne diseases:an analysis.VectorBorne and Zoonotic Diseases,10:295-311.
    Alphey L,Nimmo D,O'Connell S and Alphey N.2008.Insectpopulation suppression using engineered insects∥Aksoy S.Transgenesis and the Management of Vector-Borne Disease.Austin,Texas:Landes Bioscience,93-103.
    Alphey N,Alphey L and Bonsall M B.2011.A model framework to estimate impact and cost of genetics-based sterile insect methods for dengue vector control.PLoS ONE,6:e25384.
    Arensburger P,Kim Y J,Orsetti J,Aluvihare C,O'Brochta DA and Atkinson P W.2005.An active transposable element,Herves,from the African malaria mosquito Anopheles gambiae.Genetics,169:697-708.
    Asman S M,Nelson R L and McD onald P T.1979.Pilot release of sex-linked multiple translocation into a Culex tarsalisfield population in Kern County,California.Mosquito Systematics,39:248-258.
    Asman S M,Zalom F G and Meyer R P.1980.A field releaseof irradiated male Culex tarsalis in California∥Grant C D.Proceedings and Papers of the 48th Annual Conference of theCalifornia Mosquito and Vector Control Association,Inc.Anaheim,California:CMVCA Press,64.
    Atkinson M P,Su Z,Alphey N,Alphey L S,Coleman P G andWein L M.2007.Analyzing the control of mosquito-bornediseases by a dominant lethal genetic system.Proceedings ofthe National Academy of Sciences of the United States of America,104:9540-9545.
    Baker R H,Reisen W K,Sakai R K,Hayes C G,Aslamkhan M,Saifuddin U T,Mahmood F,Perveen A and Javed S.1979.Field assessment of mating competitiveness of male Culex tritaeniorhynchus carrying a complex chromosomal aberration.Annalsof the Entomological Society of America,72:751-758.
    Baker R H,Reisen W K,Sakai R K,Rathor H R,Raana K,Azra K and Niaz S.1980.Anopheles culicifacies:matingbehavior and competitiveness in nature of males carrying acomplex chromosomal aberration.Annals of the Entomological Society of America,73:581-588.
    Bargielowski I,Alphey L and Koella J C.2011a.Cost of mating and insemination capacity of a genetically modified mosquito Aedes aegypti OX513A compared to its wild type counterpart.PLoS ONE,6:e26086.
    Bargielowski I,Kaufmann C,Alphey L,Reiter P and Koella J.2012.Flight performance and teneral energy reserves of twogenetically-modified and one wild-type strain of the yellow fever mosquito Aedes aegypti.Vector-Borne and Zoonotic Diseases,12:1053-1058.
    Bargielowski I,Nimmo D,Alphey L and Koella J C.2011b.Comparison of life history characteristics of the geneticallymodified OX513A line and a wild type strain of Aedes aegypti.PLoS ONE,6:e20699.
    Benedict M Q and Robinson A S.2003.The first releases oftransgenic mosquitoes:an argument for the sterile insecttechnique.Trends in Parasitology,19:349-355.
    Bian G,Joshi D,Dong Y,Lu P,Zhou G L,Pan X L,Xu Y,Dimopoulos G and Xi Z Y.2013.Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection.Science,340:748-751.
    Bian G,Xu Y,Lu P,Xie Y and Xi Z Y.2010.The endosymbiotic bacterium Wolbachia induces resistance to Dengue virusin Aedes aegypti.PLoS Pathogens,6:e1000833.
    Black W C,Alphey L and James A A.2011.Why RIDL is notSIT.Trends in Parasitology,27:362-370.
    Breeland S G,Jeffery G M,Lofgren C S and Weidhaas D E.1974.Release of chemosterilized males for the control of Anopheles albimanus in El Salvador I.Characteristics of thetest site and the natural population.The American Journal ofTropical Medicine and Hygiene,23:274-281.
    Brennan L J,Keddie B A,Braig H R and Harris H L.2008.The endosymbiont Wolbachia pipientis induces the expressionof host antioxidant proteins in an Aedes albopictus cell line.PLoS ONE,3:e2083.
    Burt A.2003.Site-specific selfish genes as tools for the controland genetic engineering of natural populations.Proceedingsof the Royal Society of London.Series B:Biological Sciences,270:921-928.
    Catteruccia F,Benton J P and Crisanti A.2005.An Anophelestransgenic sexing strain for vector control.Nature Biotechnology,23:1414-1417.
    Catteruccia F,Crisanti A and Wimmer E A.2009.Transgenictechnologies to induce sterility.Malaria Journal,8(Suppl2):S7.
    Catteruccia F,Godfray H C J and Crisanti A.2003.Impact ofgenetic manipulation on the fitness of Anopheles stephensimosquitoes.Science,299:1225-1227.
    Catteruccia F,Nolan T,Blass C,Müller H M,Crisanti A,Kafatos F C and Loukeris T G.2000a.Toward Anophelestransformation:Minos element activity in anopheline cellsand embryos.Proceedings of the National Academy of Sciences of the United States of America,97:2157-2162.
    Catteruccia F,Nolan T,Loukeris T G,Blass C,Savakis C,Kafatos F C and Crisanti A.2000b.Stable germline transformation of the malaria mosquito Anopheles stephensi.Nature,405:959-962.
    Chen C H,Huang H X,Ward C M,Su J T,Schaeffer L V,Guo M and Hay B A.2007.A synthetic maternal-effect selfish genetic element drives population replacement in Drosophila.Science,316:597-600.
    Coates C J,Jasinskiene N,Miyashiro L and James A A.1998.Mariner transposition and transformation of the yellow fever mosquito,Aedes aegypti.Proceedings of the National Academy ofSciences of the United States of America,95:3748-3751.
    Cousserans J and Guille G.1974.Expérience de lutte genetique contre Culex pipiens dans la région deM ontpellier.Synthèse de quatre annèes de'observations.Bulletin Biologique,108:253-257.
    Curtis C F.1968.Possible use of translocations to fix desirablegenes in insect pest populations.Nature,218:368-369.
    Curtis C F,Brooks G D,Ansari M A,Grover K K,Krishnamurthy B S,Rajagopalan P K,Sharma L S,Sharma V P,Singh D,Singh K R P and Yasuno M.1982.A field trial oncontrol of Culex quinquefasciatus by release of males of astrain integrating cytoplasmic incompatibility and a translocation.Entomologia Experimentalis et Applicata,31(2-3):181-190.
    Dame D A,Lowe R E and Williamson D L.1981.Assessmentof released sterile Anopheles albimanus and Glossina morsitans morsitans∥Pal R,Kitzmiller J B and Kanda T.Cytogenetics and Genetics of Vectors:Proceedings of A Symposium ofthe 16th International Congress of Entomology.Amsterdam,Netherlands:Elsevier Biomedical Press,231-248.
    Dame D A,Woodard D B,Ford H R and Weidhaas D E.1964.Field behavior of sexually sterile Anopheles quadrimaculatus males.Mosquito News,24:6-14.
    Davidson G,Odetoyinbo J A,Colussa B and Coz J.1970.Afield attempt to assess the mating competitiveness of sterilemales produced by crossing 2 members of the Anopheles gambiae complex.Bulletin of the World Health Organization,42:55-67.
    Davis S,Bax N and Grewe P.2001.Engineered underdominanceallows efficient and economic introgression of traits into pestpopulations.Journal of Theoretical Biology,212:83-98.
    Deredec A,Burt A and Godfray H C J.2008.Population genetics of using homing endonuclease genes in vector and pestmanagement.Genetics,179:2013-2026.
    Fay R W and Craig G B.1969.Genetically marked Aedes aegypti in studies of field populations.Mosquito News,29:121-127.
    Fraser M J,Smith G E and Summers M D.1983.Acquisitionof host cell DNA sequences by Baculoviruses:relationshipbetween host DNA insertions and FP mutants of Autographacalifornica and Galleria mellonella nuclear polyhedrosis viruses.Journal of Virology,47:287-300.
    Fu G L,Lees R S,Nimmo D,Aw D,Jin L,Gray P,Berendonkb T U,White-Cooper H,Scaifea S,Phuc H K,Marinotti O,Jasinskiene N,James A A and Alphey L.2010.Female-specific flightless phenotype for mosquito control.Proceedings of the National Academy of Sciences of the United States of America,107:4550-4554.
    Galizi R,Doyle L A,Menichelli M,Bernardini F,Deredec A,Burt A,Stoddard B L,Windbichler N and Crisanti A.2014.A synthetic sex ratio distortion system for the controlof the human malaria mosquito.Nature Communications,5:3977,doi:10.1038/ncomms4977.
    Gong P,Epton M J,Fu G L,Scaife S,Hiscox A,Condon KC,Condon G C,Morrison N I,Kelly D W,Dafa'alla T,Coleman P G and Alphey L.2005.A dominant lethal genetic system for autocidal control of the Mediterranean fruit fly.Nature Biotechnology,23:453-456.
    Grover K K,Curtis C F,Sharma V P,Singh K R P,Dietz K,Agarwal H V,Razdan R K and Vaidyanathan V.1976a.Competitiveness of chemosterilised males and cytoplasmicallyincompatible translocated males of Culex pipiens fatigansWiedemann(Diptera,Culicidae)in the field.Bulletin ofEntomological Research,66:469-480.
    Grover K K,Suguna S G,Uppal D K,Singh K R P,Ansari MA,Curtis C F,Singh D,Sharma V P and Panicker K N.1976b.Field experiments on the competitiveness of malescarrying genetic control systems for Aedes aegypti.Entomologia Experimentalis et Applicata,20:8-18.
    Hancock P A and Godfray H C J.2012.Modelling the spreadof Wolbachia in spatially heterogeneous environments.Journal of the Royal Society Interface,9:3045-3054.
    Handler A M.2002.Use of the piggyB ac transposon for germline transformation of insects.Insect Biochemistry and Molecular Biology,32:1211-1220.
    Hanson S M,Mutebi J P,Craig G B J and Novak R J.1993.Reducing the overwintering ability of Aedes albopictus bymale release.Journal of the American Mosquito Control Association,9:78-83.
    Harris A F,McK emey A R,Nimmo D,Curtis Z,Black I,Morgan S A,Oviedo M N,Lacroix R,et al.2012.Successful suppression of a field mosquito population by sustainedrelease of engineered male mosquitoes.Nature Biotechnology,30:828-830.
    Harris A F,Nimmo D,McK emey A R,Kelly N,Scaife S,Donnelly C A,Beech C,Petrie W D and Alphey L.2011.Field performance of engineered male mosquitoes.Nature Biotechnology,29:1034-1037.
    Hendrichs J,Robinson A S,Cayol J P and Enkerlin W.2002.Medfly areawide sterrile insect technique programmes for prevention,suppression or eradication:the importance of mating behavior studies.Florida Entomologist,85:1-13.
    Irvin N,Hoddle M S,O'Brochta D A,Carey B and Atkinson PW.2004.Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes.Proceedings of the National Academy of Sciences of the United States ofAmerica,101:891-896.
    Jasinskiene N,Coates C J,Benedict M Q,Cornel A J,Rafferty CS,James A A and Collins F H.1998.Stable transformation ofthe yellow fever mosquito,Aedes aegypti,with the Hermes element from the housefly.Proceedings of the National Academy ofSciences of the United States of America,95:3743-3747.
    Klassen W.2009.Introduction:development of the sterile insect technique for African malaria vectors.Malaria Journal,8(Suppl 2):11.
    Knipling E F.1970.Suppression of pest Lepidoptera by releasing partially sterile males:a theoretical appraisal.Bioscience,20:465-470.
    LabbéG M C,Scaife S,Morgan S A,Curtis Z H and AlpheyL.2012.Female-specific flightless(fsRIDL)phenotype forcontrol of Aedes albopictus.PLoS Neglected Tropical Diseases,6:e1724.
    Lacroix R,McK emey A R,Raduan N,Wee L K,Ming W H,Ney T G,Rahidah A A S,Salman S,et al.2012.Openfield release of genetically engineered sterile male Aedes aegypti in Malaysia.PLoS ONE,7:e42771.
    Laven H.1967.Eradication of Culex pipiens fatigans throughcytoplasmic incompatibility.Nature,216:383-384.
    Laven H,Cousserans J and Guille G.1972.Eradicating mosquitoes using translocations:a first field experiment.Nature,236:456-457.
    Lee H L,Joko H,Nazni W A and Vasan S S.2009.Comparative life parameters of transgenic and wild strain of Aedes aegypti in the laboratory.Dengue Bulletin,33:103-114.
    Lee H L,Vasan S,Ahmad N W,Idris I,Hanum N,Selvi S,Alphey L and Murad S.2013.Mating compatibility and competitiveness of transgenic and wild type Aedes aegypti(L.)under contained semi-field conditions.Transgenic Research,22:47-57.
    Magori K and Gould F.2006.Genetically engineered underdominance for manipulation of pest populations:a deterministic model.Genetics,172:2613-2620.
    Marrelli M T,Moreira C K,Kelly D and Jacobs-Lorena M.2006.Mosquito transgenesis:what is the fitness costTrends in Parasitology,22:197-202.
    Massonnet-Bruneel B,Corre-Catelin N,Lacroix R,Lees R S,Hoang K P,Nimmo D,Alphey L and Reiter P.2013.Fitness of transgenic mosquito Aedes aegypti males carrying adominant lethal genetic system.PLoS ONE,8:e62711.
    McD onald P T,Hausermann W and Lorimer N.1977.Sterility introduced by release of genetically altered males to a domesticpopulation of Aedes aegypti at the Kenya coast.The AmericanJournal of Tropical Medicine and Hygiene,26:553-561.
    Milby M M.1980.Release of heterozygous translocated adultales for genetic control of Culex tarsalis at an isolated site.Mosquito Systematics,40:83-90.
    Moreira L A,Iturbe-Ormaetxe I,Jeffery J A,Lu G,Pyke A T,Hedges L M,Rocha B C,Hall-Mendelin S,et al.2009.AWolbachia symbiont in Aedes aegypti limits infection with dengue,Chikungunya,and Plasmodium.Cell,139:1268-1278.
    Morlan H B,McC ray E M J and Kilpatrick J W.1962.Fieldtests with sexually sterile males for control of Aedes aegypti.Mosquito News,22:295-300.
    Muoz D,Jimenez A,Marinotti O and James A A.2004.The AeAct-4 gene is expressed in the developing flight muscles of female Aedes aegypti.Insect Molecular Biology,13:563-568.
    Nazni W A,Selvi S,Lee H L,Sadiyah I,Azahari H,Derric N andVasan S S.2009.Susceptibility status of transgenic Aedes aegypti(L.)against insecticides.Dengue Bulletin,33:124-129.
    Nimmo D D,Alphey L,Meredith J M and Eggleston P.2006.High efficiency site-specific genetic engineering of the mosquito genome.Insect Molecular Biology,15:129-136.
    Nolan T,Papathanos P,Windbichler N,Magnusson K,BentonJ,Catteruccia F and Crisanti A.2011.Developing transgenic Anopheles mosquitoes for the sterile insect technique.Genetica,139:33-39.
    O'Brochta D A,Sethuraman N,Wilson R,Hice R H,PinkertonA C,Levesque C S,Bideshi D K,Jasinskiene N,Coates C J,James A A,Lehane M J and Atkinson P W.2003.Gene vector and transposable element behavior in mosquitoes.Journalof Experimental Biology,206:3823-3834.
    O'Connor L,Plichart C,Sang A C,Brelsfoard C L,Bossin HC and Dobson S L.2012.Open release of male mosquitoesinfected with a Wolbachia biopesticide:field performanceand infection containment.PLoS Neglected Tropical Diseases,6:e1797.
    Pan X,Zhou G,Wu J,Bian G,Lu P,Bian G,Lu P,Raikheld A S and Xi Z.2012.Wolbachia induces reactiveoxygen species(ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti.Proceedings of the National Academy of Sciences of the UnitedStates of America,109(1):E23-E31.
    Patterson R S,Ford H R,Lofgren C S and Weidhaas D E.1970a.Sterile males:their effect on an isolated population ofmosquitoes.Mosquito News,30:23-27.
    Patterson R S,Weidhaas D E,Ford H R and Lofgren C S.1970b.Suppression and elimination of an island populationof Culex pipiens quinquefasciatus with sterile males.Science,168:1368-1369.
    Petersen J L,Lounibos L P and Lorimer N.1977.Field trialsof double translocation heterozygote males for genetic controlof Aedes aegypti(L.)(Diptera:Culicidae).Bulletin of Entomological Research,67:313-324.
    Phuc H K,Andreasen M H,Burton R S,Vass C,Epton M J,Pape G,Fu G L,Condon K C,Scaife S,Donnelly C A,Coleman P G,White-Cooper H and Alphey L.2007.Lateacting dominant lethal genetic systems and mosquito control.BMC Biology,5:11.
    Rai K S,Grover K K and Suguna S G.1973.Genetic manipulation of Aedes aegypti:incorporation and maintenance of a genetic marker and a chromosomal translocation in natural populations.Bulletin of the World Health Organization,48:49-56.
    Rasgon J L and Gould F.2005.Transposable element insertionlocation bias and the dynamics of gene drive in mosquito populations.Insect Molecular Biology,14:493-500.
    Reisen W K,Baker R H,Sakai R K,Mahmood F,Rathor HR,Raana K and Toqir G.1981.Anopheles culicifaciesGiles:mating behavior and competitiveness in nature of che-mosterilized males carrying a genetic sexing system.Annalsof the Entomological Society of America,74:395-401.
    Reisen W K,Bock M E,Milby M M and Reeves W C.1985.Attempted insertion of a recessive autosomalgene into a semiisolated population of Culex tarsalis(Diptera:Culicidae).Journal of Medical Entomology,22:250-260.
    Reisen W K,Milby M M and Asman S M.1982.Attemptedsuppression of a semi-isolated Culex tarsalis population bythe release of irradiated males:a second experiment usingmales from a recently colonized strain.Mosquito News,2:565-575.
    Scolari F,Schetelig M F,Gabrieli P,Siciliano P,GomuL ski LM,Karam N,Wimmer E A,Malacrida A R and Gasperi G.2008.Insect transgenesis applied to tephritid pest control.Journal of Applied Entomology,132(9-10):820-831.
    Scott T W,Takken W,Knols B G J and Boёte C.2002.The ecology of genetically modified mosquitoes.Science,298:117-119.
    Sinkins S P and Gould F.2006.Gene drive systems for insect disease vectors.Nature Reviews Genetics,7:427-435.
    Thomas D D,Donnelly C A,Wood R J and Alphey L S.2000.Insect population control using a dominant,repressible,lethal genetic system.Science,287:2474-2476.
    Walker T,Johnson P H,Moreira L A,Iturbe-Ormaetxe I,Frentiu F D,Iturbe-Ormaetxe I,Frentiu F D,McM enimanC J,Leong Y S,Dong Y,Axford J,Kriesner P,Lloyd AL,Ritchie S A,O'Neill S L and Hoffmann A A.2011.ThewM el Wolbachia strain blocks dengue and invades caged Aedes aegypti populations.Nature,476:450-453.
    Weidhaas D E,Breeland S G,Lofgren C S,Dame D A andKaiser R.1974.Release of chemosterilized males for thecontrol of Anopheles albimanus in El Salvador IV.Dynamicsof the test population.The American Journal of TropicalMedicine and Hygiene,23:298-308.
    Weidhaas D E and Schmidt C H.1962.Field studies on the release of sterile males or the control of Anopheles quadrimaculatus.Mosquito News,22:283-291.
    Werren J H,Baldo L and Clark M E.2008.Wolbachia:master manipulators of invertebrate biology.Nature Reviews Microbiology,6:741-751.
    Wilke A B B and Marrelli M T.2012.Genetic control of mos-quitoes:population suppression strategies.Revista do Instituto de Medicina Tropical de So Paulo,54:287-292.
    Windbichler N,Menichelli M,Papathanos P A,Thyme S B,Li H,Ulge U Y,Hovde B T,Baker D,Monnat R J Jr,BurtA and Crisanti A.2011.A synthetic homing endonucleasebased gene drive system in the human malaria mosquito.Nature,473:212-215.
    Windbichler N,Papathanos P A and Crisanti A.2008.Targeting the X chromosome during spermatogenesis induces Ychromosome transmission ratio distortion and early dominantembryo lethality in Anopheles gambiae.PLoS Genetics,4:e1000291.
    Wise de Valdez M R,Nimmo D,Betz J,Gong H F and JamesA A.2011.Genetic elimination of dengue vector mosquitoes.Proceedings of the National Academy of Sciences of theUnited States of America,108:4772-4775.
    Yakob L,Alphey L and Bonsall M B.2008.Aedes aegypti control:the concomitant role of competition,space and transgenic technologies.Journal of Applied Ecology,45:1258-1265.
    Yasuno M,Macdonald W W and Curtis C F.1978.Control experiment with chemosterilized male Culex pipiens fatigansWied in a village near Delhi surrounded by a breeding-freezone.Japanese Journal of Sanitary Zoology,29:325-343.
    Zabalou S,Apostolaki A,Livadaras I,Franz G,Robinson AS,Savakis C and Bourtzis K.2009.Incompatible insecttechnique:incompatible males from a Ceratitis capitata(Diptera:Tephritidae)genetic sexing strain.Entomologia Experimentalis et Applicata,132:232-240.
    Zabalou S,Riegler M,Theodorakopoulou M,Stauffer C,Savakis C and Bourtzis K.2004.Wolbachia-induced cytoplasmicincompatibility as a means for insect pest population control.Proceedings of the National Academy of Sciences of the UnitedStates of America,101:15042-15045.
    Zhao Y G and Eggleston P.1998.Stable transformation of anAnopheles gambiae cell line mediated by the Hermes mobilegenetic element.Insect Biochemistry and Molecular Biology,28:213-219.