These authors contributed equally to this work.
Release of genetically engineered insects: a framework to identify potential ecological effects
Article first published online: 12 SEP 2013
© 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Ecology and Evolution
Volume 3, Issue 11, pages 4000–4015, October 2013
How to Cite
Ecology and Evolution 2013; 3(11): 4000–4015
- Issue published online: 9 OCT 2013
- Article first published online: 12 SEP 2013
- Manuscript Accepted: 15 JUL 2013
- Manuscript Revised: 14 JUL 2013
- Manuscript Received: 9 APR 2013
- University of Minnesota. Grant Number: DGE-0653827
- 2010. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis. 10:295–311. , , , , , , et al.
- 2011. Modeling resistance to genetic control of insects. J. Theor. Biol. 270:42–55. , , and .
- 2011. Cascading effects of bird functional extinction reduce pollination and plant density. Science 331:1068–1071. , , , , and .
- 2012. Control of the olive fruit fly using genetics-enhanced sterile insect technique. BMC Biol. 10:51. , , , , , , et al.
- 2006. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433. , , and .
- 2003. Alternative stable states in ecology. Front. Ecol. Environ. 1:376–382. , , and .
- 2009. Global status of DDT and its alternatives for use in vector control to prevent disease. Environ. Health Perspect. 117:1656–1663.
- 1997. Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow. Genetics 147:1817–1828. , , , , , , et al.
- 2003. Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation. Proc. Natl. Acad. Sci. USA 100:10818–10823. , , , , , , et al.
- 2011. Rapid evolution caused by pollinator loss in Mimulus guttatus. Evolution 65:2541–2552. , and .
- 2012. Resurrecting the ghost of green revolutions past: the brown planthopper as a recurring threat to high-yielding rice production in tropical Asia. J. Asia Pac. Entomol. 15:122–140. , and .
- 2011. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin. Microbiol. Rev. 24:377–410. , and .
- 2000. Intraguild interactions in aphid parasitoids. Entomol. Exp. Appl. 97:93–108. , and .
- 2003. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. R. Soc. Lond. B 270:921–928.
- 2003. Genetic differentiation between American and European Drosophila menalogaster populations could be attributed to admixture of African alleles. Mol. Biol. Evol. 20:792–799. , and .
- 2003. On the competition occurring between Aedes albopictus and Culex pipiens (Diptera: Culicidae) in Italy. Environ. Entomol. 32:1313–1321. , , , and .
- 2005. And the beak shall inherit – evolution in response to invasion. Ecol. Lett. 8:944–951. , , , , , and .
- 2010. Evolutionary forces on Anopheles: what makes a malaria vector? Trends Parasitol. 26:130–136. , , , and .
- 2001. Predation on immature parasitoids and its impact on aphid suppression. Oecologia 196:292–304. , and .
- 1989. Predation by birds on spruce budworm Chorisoneura fumiferana: functional, numerical, and total responses. Ecology 70:152–163. , and .
- 2010. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proc. Natl. Acad. Sci. USA 107:13777–13782. , , and .
- 2009. The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biol. Invasions 11:1107–1119. , and .
- 2012. Population dynamics of Anopheles gambiae s.l. in Bobo-Dioulasso city: bionomics, infection rate and susceptibility to insecticides. Parasit. Vector 5:127. , , , , , , et al.
- 2010. Population fluctuation of Anopheles (Diptera: Culicidae) in forest and forest edge habitats in Tucuman province, Argentina. J. Vector Ecol. 35:28–34. , , and .
- 1995. Interspecific interactions in phytophagous insects: competition revisited and resurrected. Annu. Rev. Entomol. 40:297–331. , , and .
- 2011. Requirements for effective malaria control with homing endonuclease genes. Proc. Natl. Acad. Sci. USA 108:E874–E880. , , and .
- 2002. The effect of Wolbachia-induced cytoplasmic incompatibility on host population size in natural and manipulated systems. Proc. Biol. Sci. 269:437–445. , , and .
- Dyck, V. A., J. Hendrichs, and A. S. Robinson, eds. 2005. Sterile insect technique: principles and practice in area wide integrated pest management. Springer, The Netherlands.
- 2011. The wave towards a new steady state: effects of earthworm invasion on soil microbial functions. Biol. Invasions 13:2191–2196. , , , and .
- 1990. Population dynamics of gypsy moth in North America. Annu. Rev. Entomol. 35:571–596. , and .
- EPA, US Environmental Protection Agency. 1998. Framework for ecological risk assessment. EPA Office of Research and Development, National Center for Environmental Assessment, Washington Office, Washington, DC.
- 2007. Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc. Natl. Acad. Sci. USA 104:16976–16981. , , , , and .
- 2004. Evolution of virulence. Infect. Dis. Clin. North Am. 18:1–15.
- 2011. Evolution of virulence, environmental change, and the threat posed by emerging and chronic diseases. Ecol. Res. 26:1017–1026.
- 2011. Can things get worse when an invasive species hybridizes? The harlequin ladybird Harmonia axyridis in France as a case study. Evol. Appl. 4:71–88. , , , , , and .
- 2010. Ecology: a world without mosquitoes. Nature 466:432–434.
- 2006. Earthworm invasion into previously earthworm-free temperate and boreal forests. Biol. Invasions 8:1235–1245. , , , , , , et al.
- 1998. P. 763 in Evolutionary Biology, 3rd ed. Sinauer Associates, Sunderland, MA.
- 2009. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS ONE 4:e4383. , , , , , , et al.
- 2013. Mosquito ecology and control of malaria. J. Anim. Ecol. 82:15–25. doi: 10.1111/1365-2656.12003
- 1976. Orchid pollination by Aedes mosquitoes in Alaska. Am. Midl. Nat. 95:208–210.
- 2004. Population genetics of autocidal control and strain replacement. Annu. Rev. Entomol. 49:193–217. , and .
- 2006. Genetic strategies for controlling mosquito-borne diseases. Am. Sci. 94:238–246. , , and .
- 2004. Pp. 62–65Natural enemies: an introduction to biological control. Cambridge Univ. Press, Cambridge, U.K.
- 2011. Introduced pathogens follow the invasion front of a spreading alien host. J. Anim. Ecol. 80:1217–1226. , and .
- 1995. Arthropod pest resurgence – an overview of potential mechanisms. Crop Prot. 14:3–18. , , , , , and .
- 1990. Ecology and management of the Colorado Potato Beetle. Annu. Rev. Entomol. 35:81–100.
- 1980. Effects of Urophora affinis Frfld. and U. quadrifasciate (Meig.) (Diptera: Tiphritidae on Centaurea diffusa Lam. and C. maculosa Lam. (Compositae). J. Appl. Entomol., 90:190–201. .
- 2011. Field performance of engineered male mosquitoes. Nat. Biotechnol. 29:1034–1037. , , , , , , et al.
- 2003. Consequences of recurrent gene flow from crops to wild relatives. Proc. Biol. Sci. 270:1879–1886. , , and .
- 2010. European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biol. Invasions 12:2913–2931. , , , , , , et al.
- 1975. Forest tent caterpillar in the prairie provinces. Canadian Forest Service Northern Forest Research Centre, Information Report NOR-X-135, Edmonton, Canada. , and .
- 2005. Varying degrees of Apis mellifera ligustica introgression in protected populations of the black honeybee, Apis mellifera mellifera, in northwest Europe. Mol. Ecol. 14:93–106. , , , and .
- 2000. Herd immunity and herd effect: new insights and definitions. Eur. J. Epidemiol. 16:601–606. , and .
- 2005. Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol. Lett. 8:558–574. , and .
- 2009. Ecological effects of invasive alien insects. Biol. Invasions 11:21–45. , , , , , , et al.
- 2009. Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu strictu and An. arabiensis larvae. Acta Trop. 109:118–123. , and .
- 1963. Co-existence of two related stink bugs, Nezara viridula and N. antennata under natural conditions. Res. Popul. Ecol. 5:11–22. , , and .
- 2007. Transgenic mosquitoes and the fight against malaria: managing technology push in a turbulent GMO world. Am. J. Trop. Med. Hyg. 77:232–242. , , , and .
- 2006. Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotrop. Entomol. 35:421–434. , , and .
- 2004. Eradication of the melon fly, Bactrocera cucurbitae, in Japan: importance of behavior, ecology, genetics, and evolution RID B-1570-2011. Annu. Rev. Entomol. 49:331–349. , , and .
- 2011. Predation efficiency of Anopheles gambiae larvae by aquatic predators in the western Kenya highlands. Parasit. Vector. 4:128. , , , , , , et al.
- 2008. Global spread and persistence of dengue. Ann. Rev. Microbiol. 62:71–92. , and .
- 2005. Malaria infection increases attractiveness of humans to mosquitoes. PLoS Biol. 3:e298. , , , and .
- 2012. Open field release of genetically engineered sterile male Aedes aegypti in Malaysia. PLoS ONE 7:e42771. , , , , , , et al.
- 2008. Immunity to malaria: more questions than answers. Nat. Immunol. 9:725–732. , , , and .
- 2013. Mating compatibility and competitiveness of transgenic and wild type Aedes aegypti (L.) under contained semi-field conditions. Transgenic Res. 22:47–57. doi: 10.1007/s11248-012-9625-z , , , , , , et al.
- 2005. Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J. Infect. Dis. 191:1907–1912. , , , and .
- 2009. Seasonal effects of four control methods on the invasive Morrow's Honeysuckle (Lonicera morrowii) and initial responses of understory plants in a southwestern Pennsylvania old field. Rest. Ecol. 17:549–559. , and .
- 2005. Gene flow from genetically modified rice and its environmental consequences. Bioscience 55:669–678. , and .
- 2010. Response of aspen stands to forest tent caterpillar defoliation and subsequent overstory mortality in northeastern Ontario, Canada. For. Ecol. Manage. 260:1853–1860. , and .
- 2011. Habitat heterogeneity and prey selection of Aplocheilus panchax: an indigenous larvivorous fish. J. Vector Borne Dis. 48:144–149. , , and .
- 2011. Semele: a killer-male, rescue-female system for suppression of replacement of insect disease vector populations. Genetics 187:535–551. , , , and .
- 1995. Coinfection and the evolution of parasite virulence RID A-6977-2008. Proc. Biol. Sci. 261:209–215. , and .
- 2009. The impact of transgenic mosquitoes on dengue virulence to humans and mosquitoes. Am. Nat. 174:565–577. , , , and .
- 2008. Gene flow from transgenic maize to landraces in Mexico: an analysis. Agric. Ecosyst. Environ. 123:109–115. , and .
- Millennium Ecosystem Assessment. 2005. Ecosystems and human well-being: biodiversity synthesis. World Resources Institute, Washington, DC. Available at http://www.millenniumassessment.org/documents/document.354.aspx.pdf (accessed 15 February 2013).
- 2008. Waning herd immunity: a challenge for eradication of measles. Rocky Mountain. J. Math. 38:1587–1607. , , and .
- 2007. Impact of tadpoles and mosquito larvae on ephemeral pond structure and process. Mar. Freshw. Res. 58:436–444.
- 2010. Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar. J. 9:262. , , , , , , et al.
- 2010. Risk analysis of the Australian release of Aedes aegypti (L.) (Diptera: Culicidae) containing Wolbachia. CSIRO Report, Australia. Available at: http://www.eliminatedengue.com/library/publication/document//riskanalysisfinalreportcsiro.pdf. (accessed 10 February 2013). , , , and .
- 2001. The biotic crisis and the future of evolution. Proc. Natl. Acad. Sci. USA 98:5389–5392. , and .
- 2006. Population dynamics of malaria vectors in western Kenya highlands. J. Med. Entomol., 43:200–206. , , , , , , et al.
- 2007. Problem formulation and option assessment handbook: science-guided multi-stakeholder deliberation. Pp. 1–229. ed. Ecological risk assessment of genetically engineered organisms. A publication of the GMO-ERA Project. Available at http://www.gmoera.umn.edu (accessed 21 August 2013). , and .
- 1988. Larval consumption rates, interspecific predation, and local guild composition of egg-overwintering Agabus (Coleoptera, Dytiscidae) species in vernal ponds. Oecologia 76:131–137. , and .
- NRC, United States National Research Council. 2002. Animal biotechnology: science-based concerns. The National Academies Press, Washington, DC.
- 2013. Breakdown in the process of incipient speciation in Anopheles Gambiae. Genetics 193:1221–1231. , , , , , , et al.
- 2006. Dengue prevention and 35 years of vector control in Singapore. Emerg. Infect. Dis. 12:887–893. , , and .
- 2004. Effects of biological control agents and exotic plant invasion on deer mouse populations. Ecol. Appl. 14:241–253. , , and .
- 2006. Biological control agents elevate hantavirus by subsidizing deer mouse populations. Ecol. Lett. 9:443–450. , and .
- 2006. Pp. 371–372 in Entomology and pest management, 5th ed. Pearson Education, Inc., Upper Saddle River, New Jersey, NY. , and .
- 1995. Impact of tent caterpillar defoliation on the reproductive success of black-capped chickadees. Condor 97:1071–1074. , and .
- 1996. Challenges in the quest for keystones. Bioscience 46:609–620. , , , , , , et al.
- 2011. Pyrethroid resistance in African anopheline mosquitoes: what are the implications for malaria control? Trends Parasitol. 27:91–98. , , , , , and .
- 2004. Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshw. Biol. 49:274–285. , , , , and .
- 2009. Experimental assessment of the impacts of northern long-eared bats on ovipositing Culex (Diptera: Culicidae) mosquitoes. J. Med. Entomol. 46:1037–1044. , and .
- 1994. Mitochondrial analysis of gene flow between New Zealand mallards (Anas platyrhynchos) and grey ducks (A. superciliosa). Auk 11:970–978. , , and .
- 1984. Population dynamics of the spruce budworm Choristoneura fumiferana. Ecol. Monogr. 54:429–462.
- 2011. The influence of amphibians on mosquitoes in seasonal pools: can wetlands protection help to minimize disease risk? Wetlands 31:799–804. , , , and .
- 2011. Strong contributors to network persistence are the most vulnerable to extinction. Nature 478:233–236. , , , and .
- 2007. Ecological and evolutionary insights from species invasions RID A-7423-2008 RID F-2275-2010. Trends Ecol. Evol. 22:465–471. , , , , , , et al.
- 2009. Aquatic insect predators and mosquito control. Trop. Biomed. 26:223–261. , and .
- 1985. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16:393–430.
- 2005. Genetically engineered organisms and the environment: current status and recommendations. Ecol. Appl. 15:377–404. , , , , , , et al.
- 2006. Ecological effects of invasive arthropod generalist predators. Annu. Rev. Ecol. Evol. Syst. 37:95–122. , and .
- 2000. Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716. , and .
- 2008. Insect resistance to Bt crops: evidence versus theory. Nat. Biotechnol. 26:199–202. , , , and .
- 1989. The planned introduction of genetically engineered organisms: ecological considerations and recommendations. Ecology 70:298–315. , , , , , , et al.
- 2005. Dynamic models of meningococcal carriage, disease, disease and the impact of serogroup C conjugate vaccination. Am. J. Epidemiol. 162:89–100. , , and .
- 2011. Sequential adaptive mutations enhance efficient vector switching by Chikungunya virus and its epidemic emergence. PLoS Pathog. 7: e1002412. doi: 10.1371/journal.ppat.1002412 , and .
- USDA, United States Department of Agriculture. 2008. Use of genetically engineered fruit fly and pink bollworm in APHIS plant pest control programs: final Environmental Impact Statement. USDA, Riverdale, MD. Available at http://www.aphis.usda.gov/plant_health/ea/downloads/eis-gen-pbw-ff.pdf. (accessed 15 February 2013).
- USFWS, United States Fish and Wildlife Service. 2005. Interim mosquito guidance. FWS/ANRS-NR-WR/02 0301. Available at http://www.fws.gov/cno/refuges/DonEdwards/CCP-PDFs/Appendix-K4_EffectsofMosquitoControl.pdf. (accessed 15 February 2013).
- 2009. Effects of spruce budworm (Choristoneura fumiferana (Clem.)) outbreaks on boreal mixed-wood bird communities. Avian Conserv. Ecol. 4. Available at: http://www.ace-eco.org/vol4/iss1/art3. (accessed 13 February 2013). , , , , and .
- 2011. The first large-scale use of synthetic insecticide for malaria control in tropical africa: lessons from Liberia, 1945–1962. J. Hist. Med. Allied Sci. 66:347–376. .
- 1991. Interspecific gene flow in sympatric oaks. Proc. Natl. Acad. Sci. USA 88:2540–2544. , and .
- WHO, World Health Organization. 2012. World Malaria Report. Available at http://www.who.int/malaria/publications/world_malaria_report_2012/report/en/index.html. (accessed 2 July 2013).
- 2008. Targeting the x chromosome during spermatogenesis induces y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae. PLoS Genet. 4:e1000291. doi: 10.1371/journal.pgen.1000291 , , and .
- 2011. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212–217. , , , , , , et al.
- 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Pp. 356–366 in D. F. Jones, ed. Proceedings of the sixth international congress of genetics. Brooklyn Botanic Garden, Brooklyn, NY.
- 2012. Crossing the divide: gene flow produces intergeneric hybrid in feral transgenic creeping bentgrass population. Mol. Ecol. 21:4672–4680. , and .