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Published in: Malaria Journal 1/2005

Open Access 01-12-2005 | Research

Fitness consequences of Anopheles gambiae population hybridization

Authors: David M Menge, Tom Guda, Daibin Zhong, Aditi Pai, Goufa Zhou, John C Beier, Louis Gouagna, Guiyun Yan

Published in: Malaria Journal | Issue 1/2005

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Abstract

Background

The use of transgenic mosquitoes with parasite inhibiting genes has been proposed as an integral strategy to control malaria transmission. However, release of exotic transgenic mosquitoes will bring in novel alleles along with parasite-inhibiting genes that may have unknown effects on native populations. Thus it is necessary to study the effects and dynamics of fitness traits in native mosquito populations in response to the introduction of novel genes. This study was designed to evaluate the dynamics of fitness traits in a simulation of introduction of novel alleles under laboratory conditions using two strains of Anopheles gambiae: Mbita strain from western Kenya and Ifakara strain from Tanzania.

Methods

The dynamics of fitness traits were evaluated under laboratory conditions using the two An. gambiae strains. These two geographically different strains were cross-bred and monitored for 20 generations to score fecundity, body size, blood-meal size, larval survival, and adult longevity, all of which are important determinants of the vector's potential in malaria transmission. Traits were analysed using pair-wise analysis of variance (ANOVA) for fecundity, body size, and blood-meal size while survival analysis was performed for larval survival and adult longevity.

Results

Fecundity and body size were significantly higher in the progeny up to the 20th generation compared to founder strains. Adult longevity had a significantly higher mean up to the 10th generation and average blood-meal size was significantly larger up to the 5th generation, indicating that hybrids fitness is enhanced over that of the founder strains.

Conclusion

Hybridization of the two mosquito populations used in this study led to increased performance in the fitness traits studied. Given that the studied traits are important determinants of the vector's potential to transmit malaria, these results suggest the need to release genetically modified mosquitoes that have the same or very similar backgrounds to the native populations.
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Literature
1.
go back to reference Breman JG: The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg. 2001, 64: 1-11.PubMed Breman JG: The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg. 2001, 64: 1-11.PubMed
2.
go back to reference Gallup JL, Sachs JD: The economic burden of malaria. Am J Trop Med Hyg. 2001, 6: 84-96. Gallup JL, Sachs JD: The economic burden of malaria. Am J Trop Med Hyg. 2001, 6: 84-96.
3.
go back to reference Breman JG, Alilio M, Mills A: Conquering the intolerable burden of malaria: What's new, What's needed: A summary. Am J Trop Med Hyg. 2004, 71: 1-15.PubMed Breman JG, Alilio M, Mills A: Conquering the intolerable burden of malaria: What's new, What's needed: A summary. Am J Trop Med Hyg. 2004, 71: 1-15.PubMed
5.
go back to reference Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M: Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature. 2002, 417: 452-455. 10.1038/417452a.CrossRefPubMed Ito J, Ghosh A, Moreira LA, Wimmer EA, Jacobs-Lorena M: Transgenic anopheline mosquitoes impaired in transmission of a malaria parasite. Nature. 2002, 417: 452-455. 10.1038/417452a.CrossRefPubMed
6.
go back to reference Moreira LA, Jing W, Frank HC, Jacobs-Lorena M: Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics. 2004, 166: 1337-1341. 10.1534/genetics.166.3.1337.PubMedCentralCrossRefPubMed Moreira LA, Jing W, Frank HC, Jacobs-Lorena M: Fitness of anopheline mosquitoes expressing transgenes that inhibit Plasmodium development. Genetics. 2004, 166: 1337-1341. 10.1534/genetics.166.3.1337.PubMedCentralCrossRefPubMed
7.
go back to reference Catteruccia F, Godfray HC, Crisanti A: Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science. 2003, 299: 1225-1227. 10.1126/science.1081453.CrossRefPubMed Catteruccia F, Godfray HC, Crisanti A: Impact of genetic manipulation on the fitness of Anopheles stephensi mosquitoes. Science. 2003, 299: 1225-1227. 10.1126/science.1081453.CrossRefPubMed
8.
go back to reference Jasinskiene N, Coates CJ, Benedicts MQ, Cornel AJ, Rafferty CS, James AA, Collins FH: Stable transposon-mediated transformation of yellow fever mosquito Aedes aegypti, using the Hermes element from the housefly. Proc Natl Acad Sci USA. 1998, 95: 3743-3747. 10.1073/pnas.95.7.3743.PubMedCentralCrossRefPubMed Jasinskiene N, Coates CJ, Benedicts MQ, Cornel AJ, Rafferty CS, James AA, Collins FH: Stable transposon-mediated transformation of yellow fever mosquito Aedes aegypti, using the Hermes element from the housefly. Proc Natl Acad Sci USA. 1998, 95: 3743-3747. 10.1073/pnas.95.7.3743.PubMedCentralCrossRefPubMed
9.
go back to reference Zhao Y, Eggleston P: Stable transformation of Anopheles gambiae cell line mediated by the Hermes mobile genetic element. Insect Biochem Mol Biol. 1998, 28: 213-219. 10.1016/S0965-1748(98)00020-4.CrossRef Zhao Y, Eggleston P: Stable transformation of Anopheles gambiae cell line mediated by the Hermes mobile genetic element. Insect Biochem Mol Biol. 1998, 28: 213-219. 10.1016/S0965-1748(98)00020-4.CrossRef
10.
go back to reference Catterucia F, Nolan T, Loukeris TS, Blass C, Savakis C, Kafatos FC, Crisanti A: Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature. 2000, 405: 959-962. 10.1038/35016096.CrossRef Catterucia F, Nolan T, Loukeris TS, Blass C, Savakis C, Kafatos FC, Crisanti A: Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature. 2000, 405: 959-962. 10.1038/35016096.CrossRef
11.
go back to reference de L Capurro L, Coleman J, Beernstsen BT, Myles KM, Olson KE, Rocha E, Krettli AU, James AA: Virus expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am J Trop Med Hyg. 2000, 4: 427-433. de L Capurro L, Coleman J, Beernstsen BT, Myles KM, Olson KE, Rocha E, Krettli AU, James AA: Virus expressed, recombinant single-chain antibody blocks sporozoite infection of salivary glands in Plasmodium gallinaceum-infected Aedes aegypti. Am J Trop Med Hyg. 2000, 4: 427-433.
12.
go back to reference Ghosh AK, Ribolla PE, Jacobs-Lorena M: Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. Proc Natl Acad Sci USA. 2001, 98: 13278-13281. 10.1073/pnas.241491198.PubMedCentralCrossRefPubMed Ghosh AK, Ribolla PE, Jacobs-Lorena M: Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. Proc Natl Acad Sci USA. 2001, 98: 13278-13281. 10.1073/pnas.241491198.PubMedCentralCrossRefPubMed
13.
go back to reference Zieler H, Keister DB, Dvorak JA, Ribeiro JM: A snake venom phospholipase A(2) blocks malaria parasite development in the mosquito midgut by inhibiting ookinete association with the midgut surface. J Exp Biol. 2001, 204: 4157-4167.PubMed Zieler H, Keister DB, Dvorak JA, Ribeiro JM: A snake venom phospholipase A(2) blocks malaria parasite development in the mosquito midgut by inhibiting ookinete association with the midgut surface. J Exp Biol. 2001, 204: 4157-4167.PubMed
14.
go back to reference Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffman JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller M, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, Mering C, Xu J, Zheng L, Bork P, Kafatos FC: Immunity-related genes and gene families in Anopheles gambiae. Science. 2002, 298: 159-165. 10.1126/science.1077136.CrossRefPubMed Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, Hetru C, Hoa NT, Hoffman JA, Kanzok SM, Letunic I, Levashina EA, Loukeris TG, Lycett G, Meister S, Michel K, Moita LF, Muller M, Osta MA, Paskewitz SM, Reichhart JM, Rzhetsky A, Troxler L, Vernick KD, Vlachou D, Volz J, Mering C, Xu J, Zheng L, Bork P, Kafatos FC: Immunity-related genes and gene families in Anopheles gambiae. Science. 2002, 298: 159-165. 10.1126/science.1077136.CrossRefPubMed
15.
go back to reference Osta MA, Christophides GK, Kafatos FC: Effects of mosquito genes on Plasmodium development. Science. 2004, 303: 2030-2032. 10.1126/science.1091789.CrossRefPubMed Osta MA, Christophides GK, Kafatos FC: Effects of mosquito genes on Plasmodium development. Science. 2004, 303: 2030-2032. 10.1126/science.1091789.CrossRefPubMed
16.
go back to reference James AA: Blocking malaria parasite invasion of mosquito salivary glands. J Exp Biol. 2003, 206: 3817-3821. 10.1242/jeb.00616.CrossRefPubMed James AA: Blocking malaria parasite invasion of mosquito salivary glands. J Exp Biol. 2003, 206: 3817-3821. 10.1242/jeb.00616.CrossRefPubMed
17.
go back to reference Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL: The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002, 298: 129-149. 10.1126/science.1076181.CrossRefPubMed Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, Wides R, Salzberg SL, Loftus B, Yandell M, Majoros WH, Rusch DB, Lai Z, Kraft CL, Abril JF, Anthouard V, Arensburger P, Atkinson PW, Baden H, de Berardinis V, Baldwin D, Benes V, Biedler J, Blass C, Bolanos R, Boscus D, Barnstead M, Cai S, Center A, Chaturverdi K, Christophides GK, Chrystal MA, Clamp M, Cravchik A, Curwen V, Dana A, Delcher A, Dew I, Evans CA, Flanigan M, Grundschober-Freimoser A, Friedli L, Gu Z, Guan P, Guigo R, Hillenmeyer ME, Hladun SL, Hogan JR, Hong YS, Hoover J, Jaillon O, Ke Z, Kodira C, Kokoza E, Koutsos A, Letunic I, Levitsky A, Liang Y, Lin JJ, Lobo NF, Lopez JR, Malek JA, McIntosh TC, Meister S, Miller J, Mobarry C, Mongin E, Murphy SD, O'Brochta DA, Pfannkoch C, Qi R, Regier MA, Remington K, Shao H, Sharakhova MV, Sitter CD, Shetty J, Smith TJ, Strong R, Sun J, Thomasova D, Ton LQ, Topalis P, Tu Z, Unger MF, Walenz B, Wang A, Wang J, Wang M, Wang X, Woodford KJ, Wortman JR, Wu M, Yao A, Zdobnov EM, Zhang H, Zhao Q, Zhao S, Zhu SC, Zhimulev I, Coluzzi M, della Torre A, Roth CW, Louis C, Kalush F, Mural RJ, Myers EW, Adams MD, Smith HO, Broder S, Gardner MJ, Fraser CM, Birney E, Bork P, Brey PT, Venter JC, Weissenbach J, Kafatos FC, Collins FH, Hoffman SL: The genome sequence of the malaria mosquito Anopheles gambiae. Science. 2002, 298: 129-149. 10.1126/science.1076181.CrossRefPubMed
18.
go back to reference Yan G, Serverson DW, Christensen BM: Costs and benefits of mosquito refractoriness to malaria parasites: Implications for the genetic variability of mosquitoes and genetic control of malaria. Evolution. 1997, 5: 441-450.CrossRef Yan G, Serverson DW, Christensen BM: Costs and benefits of mosquito refractoriness to malaria parasites: Implications for the genetic variability of mosquitoes and genetic control of malaria. Evolution. 1997, 5: 441-450.CrossRef
19.
go back to reference Braig HR, Yan G: The spread of genetic constructs in natural insect populations. Genetically engineered organisms: Assessing environmental and human health effects. 2001, Letourneau CRS Press, 251-314. Braig HR, Yan G: The spread of genetic constructs in natural insect populations. Genetically engineered organisms: Assessing environmental and human health effects. 2001, Letourneau CRS Press, 251-314.
20.
go back to reference Yan G, Severson DW: Dynamics of molecular markers linked to the resistance loci in a mosquito-Plasmodium system. Genetics. 2003, 164: 511-519.PubMedCentralPubMed Yan G, Severson DW: Dynamics of molecular markers linked to the resistance loci in a mosquito-Plasmodium system. Genetics. 2003, 164: 511-519.PubMedCentralPubMed
21.
go back to reference Dobson SL, Marsland EJ, Rattanadechakul W: Wolbachia induced cytoplasmic incompatibility in single and superinfected Aedes albopictus (Diptera: Culicidae). J Med Entomol. 2001, 38: 382-387.CrossRefPubMed Dobson SL, Marsland EJ, Rattanadechakul W: Wolbachia induced cytoplasmic incompatibility in single and superinfected Aedes albopictus (Diptera: Culicidae). J Med Entomol. 2001, 38: 382-387.CrossRefPubMed
22.
go back to reference Ward RA: Genetics aspects of the susceptibility of mosquitoes to malaria infection. Exp Parasitol. 1963, 13: 328-341. 10.1016/0014-4894(63)90084-5.CrossRefPubMed Ward RA: Genetics aspects of the susceptibility of mosquitoes to malaria infection. Exp Parasitol. 1963, 13: 328-341. 10.1016/0014-4894(63)90084-5.CrossRefPubMed
23.
go back to reference Kelly R, Edman JD: Mosquito size and multiple transmission of avian malaria in the laboratory. J Am Mosq Control Assoc. 1992, 8: 386-388.PubMed Kelly R, Edman JD: Mosquito size and multiple transmission of avian malaria in the laboratory. J Am Mosq Control Assoc. 1992, 8: 386-388.PubMed
24.
go back to reference Woke PA, Ally MS, Rosenberger CR: The number of eggs developed related to the quantities of human blood ingested in Aedes aegypti (L). Ann Entomol Soc Am. 1956, 49: 435-441.CrossRef Woke PA, Ally MS, Rosenberger CR: The number of eggs developed related to the quantities of human blood ingested in Aedes aegypti (L). Ann Entomol Soc Am. 1956, 49: 435-441.CrossRef
25.
go back to reference Kershaw WE, Lavoipierre JMM, Beesley WN: Studies on the intake of microfilariae by their insect vectors. VII. Further observations on the intake of microfilariae of Dirofilaria immitis by Aedes aegypti in laboratory conditions: The pattern of the intake of a group of flies. Ann Trop Med Parasitol. 1955, 49: 203-211.PubMed Kershaw WE, Lavoipierre JMM, Beesley WN: Studies on the intake of microfilariae by their insect vectors. VII. Further observations on the intake of microfilariae of Dirofilaria immitis by Aedes aegypti in laboratory conditions: The pattern of the intake of a group of flies. Ann Trop Med Parasitol. 1955, 49: 203-211.PubMed
26.
go back to reference Briegel H, Lea AO, Klowden MJ: Hemoglobinometry as a method for measuring blood meal sizes of mosquitoes. J Med Entomol. 1979, 15: 235-238.CrossRef Briegel H, Lea AO, Klowden MJ: Hemoglobinometry as a method for measuring blood meal sizes of mosquitoes. J Med Entomol. 1979, 15: 235-238.CrossRef
27.
go back to reference Shull GH: Beginnings of the heterosis concept. Edited by: John Gowan. 1952, Heterosis Ames: Iowa State College Press, 14-48. Shull GH: Beginnings of the heterosis concept. Edited by: John Gowan. 1952, Heterosis Ames: Iowa State College Press, 14-48.
28.
go back to reference Bruce CLJ: Essentials of malariology. 1985, New York: John Wiley and Sons, Second Bruce CLJ: Essentials of malariology. 1985, New York: John Wiley and Sons, Second
29.
go back to reference Molineaux L: The epidemiology of human malaria as an expression of its distribution including some implications for its control. Malaria, principles and practice of malariology. 1988, London: Churchill Livingston, 2: 913-998. Molineaux L: The epidemiology of human malaria as an expression of its distribution including some implications for its control. Malaria, principles and practice of malariology. 1988, London: Churchill Livingston, 2: 913-998.
Metadata
Title
Fitness consequences of Anopheles gambiae population hybridization
Authors
David M Menge
Tom Guda
Daibin Zhong
Aditi Pai
Goufa Zhou
John C Beier
Louis Gouagna
Guiyun Yan
Publication date
01-12-2005
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2005
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-4-44

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