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PLOS ONE  2014 

Transgenic Anopheles gambiae Expressing an Antimalarial Peptide Suffer No Significant Fitness Cost

DOI: 10.1371/journal.pone.0088625

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Abstract:

Mosquito-borne diseases present some of the greatest health challenges faced by the world today. In many cases, existing control measures are compromised by insecticide resistance, pathogen tolerance to drugs and the lack of effective vaccines. In light of these difficulties, new genetic tools for disease control programmes, based on the deployment of genetically modified mosquitoes, are seen as having great promise. Transgenic strains may be used to control disease transmission either by suppressing vector populations or by replacing susceptible with refractory genotypes. In practice, the fitness of the transgenic strain relative to natural mosquitoes will be a critical determinant of success. We previously described a transgenic strain of Anopheles gambiae expressing the Vida3 peptide into the female midgut following a blood-meal, which exhibited significant protection against malaria parasites. Here, we investigated the fitness of this strain relative to non-transgenic controls through comparisons of various life history traits. Experiments were designed, as far as possible, to equalize genetic backgrounds and heterogeneity such that fitness comparisons focussed on the presence and expression of the transgene cassette. We also employed reciprocal crosses to identify any fitness disturbance associated with inheritance of the transgene from either the male or female parent. We found no evidence that the presence or expression of the effector transgene or associated fluorescence markers caused any significant fitness cost in relation to larval mortality, pupal sex ratio, fecundity, hatch rate or longevity of blood-fed females. In fact, fecundity was increased in transgenic strains. We did, however, observe some fitness disturbances associated with the route of inheritance of the transgene. Maternal inheritance delayed male pupation whilst paternal inheritance increased adult longevity for both males and unfed females. Overall, in comparison to controls, there was no evidence of significant fitness costs associated with the presence or expression of transgenes in this strain.

References

[1]  Ranson H, Abdallah H, Badolo A, Guelbeogo WM, Kerah-Hinzoumbe C, et al. (2009) Insecticide resistance in Anopheles gambiae: data from the first year of a multi-country study highlight the extent of the problem. Malar J 8: 299. doi: 10.1186/1475-2875-8-299
[2]  Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M (2002) Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature 417: 452–455. doi: 10.1038/417452a
[3]  Moreira LA, Ito J, Ghosh A, Devenport M, Zieler H, et al. (2002) Bee venom phospholipase inhibits malaria parasite development in transgenic mosquitoes. J Biol Chem 277: 40839–40843. doi: 10.1074/jbc.m206647200
[4]  Abraham EG, Pinto SB, Ghosh A, Vanlandingham DL, Budd A, et al. (2005) An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci U S A 102: 16327–16332. doi: 10.1073/pnas.0508335102
[5]  Yoshida S, Shimada Y, Kondoh D, Kouzuma Y, Ghosh AK, et al. (2007) Hemolytic C-type lectin CEL-III from sea cucumber expressed in transgenic mosquitoes impairs malaria parasite development. PLoS Pathog 3: e192. doi: 10.1371/journal.ppat.0030192
[6]  Corby-Harris V, Drexler A, Watkins de Jong L, Antonova Y, Pakpour N, et al. (2010) Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog 6: e1001003. doi: 10.1371/journal.ppat.1001003
[7]  Rodrigues FG, Santos MN, de Carvalho TX, Rocha BC, Riehle MA, et al. (2008) Expression of a mutated phospholipase A2 in transgenic Aedes fluviatilis mosquitoes impacts Plasmodium gallinaceum development. Insect Mol Biol 17: 175–183. doi: 10.1111/j.1365-2583.2008.00791.x
[8]  Fu G, Lees RS, Nimmo D, Aw D, Jin L, et al. (2010) Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci U S A 107: 4550–4554. doi: 10.1073/pnas.1000251107
[9]  Meredith JM, Basu S, Nimmo DD, Larget-Thiery I, Warr EL, et al. (2011) Site-specific integration and expression of an anti-malarial gene in transgenic Anopheles gambiae significantly reduces Plasmodium infections. PLoS One 6: e14587.
[10]  Isaacs AT, Jasinskiene N, Tretiakov M, Thiery I, Zettor A, et al. (2012) Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc Natl Acad Sci U S A 109: E1922–1930.
[11]  Isaacs AT, Li F, Jasinskiene N, Chen X, Nirmala X, et al. (2011) Engineered resistance to Plasmodium falciparum development in transgenic Anopheles stephensi. PLoS Pathog 7: e1002017.
[12]  Li C, Marrelli MT, Yan G, Jacobs-Lorena M (2008) Fitness of transgenic Anopheles stephensi mosquitoes expressing the SM1 peptide under the control of a vitellogenin promoter. J Hered 99: 275–282.
[13]  Koenraadt CJ, Kormaksson M, Harrington LC (2010) Effects of inbreeding and genetic modification on Aedes aegypti larval competition and adult energy reserves. Parasit Vectors 3: 92.
[14]  Marrelli MT, Moreira CK, Kelly D, Alphey L, Jacobs-Lorena M (2006) Mosquito transgenesis: what is the fitness cost? Trends Parasitol 22: 197–202.
[15]  Moreira LA, Wang J, Collins FH, Jacobs-Lorena M (2004) Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics 166: 1337–1341.
[16]  Nimmo DD, Alphey L, Meredith JM, Eggleston P (2006) High efficiency site-specific genetic engineering of the mosquito genome. Insect Mol Biol 15: 129–136.
[17]  Grossman GL, Rafferty CS, Clayton JR, Stevens TK, Mukabayire O, et al. (2001) Germline transformation of the malaria vector, Anopheles gambiae, with the piggyBac transposable element. Insect Mol Biol 10: 597–604.
[18]  Catteruccia F, Godfray HC, Crisanti A (2003) Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science 299: 1225–1227.
[19]  O’Brochta DA, Sethuraman N, Wilson R, Hice RH, Pinkerton AC, et al. (2003) Gene vector and transposable element behaviour in mosquitoes. J Exp Biol 206: 3823–3834.
[20]  Bellen HJ, Levis RW, He Y, Carlson JW, Evans-Holm M, et al. (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188: 731–743.
[21]  Meredith JM, Underhill A, McArthur CC, Eggleston P (2013) Next-Generation Site-Directed Transgenesis in the Malaria Vector Mosquito Anopheles gambiae: Self-Docking Strains Expressing Germline-Specific phiC31 Integrase. PLoS One 8: e59264.
[22]  Marrelli MT, Li C, Rasgon JL, Jacobs-Lorena M (2007) Transgenic malaria-resistant mosquitoes have a fitness advantage when feeding on Plasmodium-infected blood. Proc Natl Acad Sci U S A 104: 5580–5583.
[23]  Amenya DA, Bonizzoni M, Isaacs AT, Jasinskiene N, Chen H, et al. (2010) Comparative fitness assessment of Anopheles stephensi transgenic lines receptive to site-specific integration. Insect Mol Biol 19: 263–269.
[24]  Dong Y, Das S, Cirimotich C, Souza-Neto JA, McLean KJ, et al. (2011) Engineered anopheles immunity to Plasmodium infection. PLoS Pathog 7: e1002458.
[25]  Bargielowski I, Nimmo D, Alphey L, Koella JC (2011) Comparison of life history characteristics of the genetically modified OX513A line and a wild type strain of Aedes aegypti. PLoS One 6: e20699.
[26]  Irvin N, Hoddle MS, O’Brochta DA, Carey B, Atkinson PW (2004) Assessing fitness costs for transgenic Aedes aegypti expressing the GFP marker and transposase genes. Proc Natl Acad Sci U S A 101: 891–896.
[27]  Arrighi RB, Nakamura C, Miyake J, Hurd H, Burgess JG (2002) Design and activity of antimicrobial peptides against sporogonic-stage parasites causing murine malarias. Antimicrob Agents Chemother 46: 2104–2110.
[28]  Groth AC, Fish M, Nusse R, Calos MP (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775–1782.
[29]  Diaz H, Ramirez AA, Olarte A, Clavijo C (2011) A model for the control of malaria using genetically modified vectors. J Theor Biol 276: 57–66.
[30]  Paaijmans KP, Wandago MO, Githeko AK, Takken W (2007) Unexpected high losses of Anopheles gambiae larvae due to rainfall. PLoS One 2: e1146.
[31]  Kirby MJ, Lindsay SW (2009) Effect of temperature and inter-specific competition on the development and survival of Anopheles gambiae sensu stricto and An. arabiensis larvae. Acta Trop 109: 118–123.
[32]  Edwards MJ, Lemos FJ, Donnelly-Doman M, Jacobs-Lorena M (1997) Rapid induction by a blood meal of a carboxypeptidase gene in the gut of the mosquito Anopheles gambiae. Insect Biochem Mol Biol 27: 1063–1072.
[33]  Diabate A, Yaro AS, Dao A, Diallo M, Huestis DL, et al. (2011) Spatial distribution and male mating success of Anopheles gambiae swarms. BMC Evol Biol 11: 184.
[34]  Koella JC, Lyimo EO (1996) Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol 33: 261–264.
[35]  Lyimo EO, Takken W (1993) Effects of adult body size on fecundity and the pre-gravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol 7: 328–332.
[36]  Hogg JC, Thomson MC, Hurd H (1996) Comparative fecundity and associated factors for two sibling species of the Anopheles gambiae complex occurring sympatrically in The Gambia. Med Vet Entomol 10: 385–391.
[37]  Okanda FM, Dao A, Njiru BN, Arija J, Akelo HA, et al. (2002) Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malar J 1: 10.
[38]  Nghabi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BGJ, et al. (2008) Sexual selection in mosquito swarms: may the best man lose? Animal Behaviour 76: 105–112.
[39]  Dao A, Kassogue Y, Adamou A, Diallo M, Yaro AS, et al. (2010) Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae). J Med Entomol 47: 769–777.
[40]  Briegel H (1990) Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), vectors of malaria. J Med Entomol 27: 839–850.
[41]  Huho BJ, Ng’habi KR, Killeen GF, Nkwengulila G, Knols BG, et al. (2007) Nature beats nurture: a case study of the physiological fitness of free-living and laboratory-reared male Anopheles gambiae s.l. J Exp Biol 210: 2939–2947.
[42]  An C, Budd A, Kanost MR, Michel K (2011) Characterization of a regulatory unit that controls melanization and affects longevity of mosquitoes. Cell Mol Life Sci 68: 1929–1939.
[43]  Lambrechts L, Morlais I, Awono-Ambene PH, Cohuet A, Simard F, et al. (2007) Effect of infection by Plasmodium falciparum on the melanization immune response of Anopheles gambiae. Am J Trop Med Hyg 76: 475–480.

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