Skip to main content
Top
Published in: Malaria Journal 1/2005

Open Access 01-12-2005 | Research

Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum

Authors: Louis Lambrechts, Jean Halbert, Patrick Durand, Louis C Gouagna, Jacob C Koella

Published in: Malaria Journal | Issue 1/2005

Login to get access

Abstract

Background

Most studies on the resistance of mosquitoes to their malaria parasites focus on the response of a mosquito line or colony against a single parasite genotype. In natural situations, however, it may be expected that mosquito-malaria relationships are based, as are many other host-parasite systems, on host genotype by parasite genotype interactions. In such systems, certain hosts are resistant to one subset of the parasite's genotypes, while other hosts are resistant to a different subset.

Methods

To test for genotype by genotype interactions between malaria parasites and their anopheline vectors, different genetic backgrounds (families consisting of the F1 offspring of individual females) of the major African vector Anopheles gambiae were challenged with several isolates of the human malaria parasite Plasmodium falciparum (obtained from naturally infected children in Kenya).

Results

Averaged across all parasites, the proportion of infected mosquitoes and the number of oocysts found in their midguts were similar in all mosquito families. Both indices of resistance, however, differed considerably among isolates of the parasite. In particular, no mosquito family was most resistant to all parasites, and no parasite isolate was most infectious to all mosquitoes.

Conclusions

These results suggest that the level of mosquito resistance depends on the interaction between its own and the parasite's genotype. This finding thus emphasizes the need to take into account the range of genetic diversity exhibited by mosquito and malaria field populations in ideas and studies concerning the control of malaria.
Appendix
Available only for authorised users
Literature
1.
go back to reference Barillas-Mury C, Wizel B, Han YS: Mosquito immune responses and malaria transmission: lessons from insect model systems and implications for vertebrate innate immunity and vaccine development. Insect Biochem Mol Biol. 2000, 30: 429-442. 10.1016/S0965-1748(00)00018-7.CrossRefPubMed Barillas-Mury C, Wizel B, Han YS: Mosquito immune responses and malaria transmission: lessons from insect model systems and implications for vertebrate innate immunity and vaccine development. Insect Biochem Mol Biol. 2000, 30: 429-442. 10.1016/S0965-1748(00)00018-7.CrossRefPubMed
2.
go back to reference Dimopoulos G: Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol. 2003, 5: 3-14. 10.1046/j.1462-5822.2003.00252.x.CrossRefPubMed Dimopoulos G: Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol. 2003, 5: 3-14. 10.1046/j.1462-5822.2003.00252.x.CrossRefPubMed
3.
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
4.
go back to reference Riehle MA, Srinivasan P, Moreira CK, Jacobs-Lorena M: Towards genetic manipulation of wild mosquito populations to combat malaria: advances and challenges. J Exp Biol. 2003, 206: 3809-3816. 10.1242/jeb.00609.CrossRefPubMed Riehle MA, Srinivasan P, Moreira CK, Jacobs-Lorena M: Towards genetic manipulation of wild mosquito populations to combat malaria: advances and challenges. J Exp Biol. 2003, 206: 3809-3816. 10.1242/jeb.00609.CrossRefPubMed
5.
go back to reference Alphey L, Beard CB, Billingsley P, Coetzee M, Crisanti A, Curtis C, Eggleston P, Godfray C, Hemingway J, Jacobs-Lorena M, James AA, Kafatos FC, Mukwaya LG, Paton M, Powell JR, Schneider W, Scott TW, Sina B, Sinden R, Sinkins S, Spielman A, Toure Y, Collins FH: Malaria control with genetically manipulated insect vectors. Science. 2002, 298: 119-121. 10.1126/science.1078278.CrossRefPubMed Alphey L, Beard CB, Billingsley P, Coetzee M, Crisanti A, Curtis C, Eggleston P, Godfray C, Hemingway J, Jacobs-Lorena M, James AA, Kafatos FC, Mukwaya LG, Paton M, Powell JR, Schneider W, Scott TW, Sina B, Sinden R, Sinkins S, Spielman A, Toure Y, Collins FH: Malaria control with genetically manipulated insect vectors. Science. 2002, 298: 119-121. 10.1126/science.1078278.CrossRefPubMed
6.
go back to reference Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW: Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science. 1986, 234: 607-610.CrossRefPubMed Collins FH, Sakai RK, Vernick KD, Paskewitz S, Seeley DC, Miller LH, Collins WE, Campbell CC, Gwadz RW: Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science. 1986, 234: 607-610.CrossRefPubMed
7.
go back to reference Niaré O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang R, Blass C, Dolo G, Bouare M, Kafatos FC, Kruglyak L, Toure YT, Vernick KD: Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science. 2002, 298: 213-216. 10.1126/science.1073420.CrossRefPubMed Niaré O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang R, Blass C, Dolo G, Bouare M, Kafatos FC, Kruglyak L, Toure YT, Vernick KD: Genetic loci affecting resistance to human malaria parasites in a West African mosquito vector population. Science. 2002, 298: 213-216. 10.1126/science.1073420.CrossRefPubMed
8.
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
9.
go back to reference Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, Kafatos FC, Levashina EA: Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell. 2004, 116: 661-670. 10.1016/S0092-8674(04)00173-4.CrossRefPubMed Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, Kafatos FC, Levashina EA: Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell. 2004, 116: 661-670. 10.1016/S0092-8674(04)00173-4.CrossRefPubMed
10.
go back to reference Scott TW, Takken W, Knols BG, Boëte C: The ecology of genetically modified mosquitoes. Science. 2002, 298: 117-119. 10.1126/science.298.5591.117.CrossRefPubMed Scott TW, Takken W, Knols BG, Boëte C: The ecology of genetically modified mosquitoes. Science. 2002, 298: 117-119. 10.1126/science.298.5591.117.CrossRefPubMed
11.
go back to reference Boëte C, Koella JC: A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J. 2002, 1: 3-10.1186/1475-2875-1-3.PubMedCentralCrossRefPubMed Boëte C, Koella JC: A theoretical approach to predicting the success of genetic manipulation of malaria mosquitoes in malaria control. Malar J. 2002, 1: 3-10.1186/1475-2875-1-3.PubMedCentralCrossRefPubMed
12.
go back to reference Norris DE, Shurtleff AC, Toure YT, Lanzaro GC: Microsatellite DNA polymorphism and heterozygosity among field and laboratory populations of Anopheles gambiae ss (Diptera: Culicidae). J Med Entomol. 2001, 38: 336-340.CrossRefPubMed Norris DE, Shurtleff AC, Toure YT, Lanzaro GC: Microsatellite DNA polymorphism and heterozygosity among field and laboratory populations of Anopheles gambiae ss (Diptera: Culicidae). J Med Entomol. 2001, 38: 336-340.CrossRefPubMed
13.
go back to reference Day KP, Koella JC, Nee S, Gupta S, Read AF: Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology. 1992, 104 Suppl: S35-52.CrossRefPubMed Day KP, Koella JC, Nee S, Gupta S, Read AF: Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology. 1992, 104 Suppl: S35-52.CrossRefPubMed
14.
go back to reference Thompson JN, Burdon JJ: Gene-for-gene coevolution between plants and parasites. Nature. 1992, 360: 121-126. 10.1038/360121a0.CrossRef Thompson JN, Burdon JJ: Gene-for-gene coevolution between plants and parasites. Nature. 1992, 360: 121-126. 10.1038/360121a0.CrossRef
15.
go back to reference Webster JP, Woolhouse MEJ: Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution. 1998, 52: 1627-1634.CrossRef Webster JP, Woolhouse MEJ: Selection and strain specificity of compatibility between snail intermediate hosts and their parasitic schistosomes. Evolution. 1998, 52: 1627-1634.CrossRef
16.
go back to reference Schmid-Hempel P, Puhr K, Krüger N, Reber C, Schmid-Hempel R: Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution. 1999, 53: 426-434.CrossRef Schmid-Hempel P, Puhr K, Krüger N, Reber C, Schmid-Hempel R: Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution. 1999, 53: 426-434.CrossRef
17.
go back to reference Carius HJ, Little TJ, Ebert D: Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution Int J Org Evolution. 2001, 55: 1136-1145.CrossRef Carius HJ, Little TJ, Ebert D: Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution Int J Org Evolution. 2001, 55: 1136-1145.CrossRef
18.
go back to reference Schmid-Hempel P, Ebert D: On the evolutionary ecology of specific immune defence. Trends in Ecology and Evolution. 2003, 18: 27-32. 10.1016/S0169-5347(02)00013-7.CrossRef Schmid-Hempel P, Ebert D: On the evolutionary ecology of specific immune defence. Trends in Ecology and Evolution. 2003, 18: 27-32. 10.1016/S0169-5347(02)00013-7.CrossRef
19.
go back to reference Kaltz O, Shykoff JA: Within- and among-population variation in infectivity, latency and spore production in a host-pathogen system. J Evol Biol. 2002, 15: 850-860. 10.1046/j.1420-9101.2002.00433.x.CrossRef Kaltz O, Shykoff JA: Within- and among-population variation in infectivity, latency and spore production in a host-pathogen system. J Evol Biol. 2002, 15: 850-860. 10.1046/j.1420-9101.2002.00433.x.CrossRef
20.
go back to reference Lynch M, Walsh B: Genetics and Analysis of Quantitative Traits. Sunderland, Massachusetts: Sinauer Associates. 1998 Lynch M, Walsh B: Genetics and Analysis of Quantitative Traits. Sunderland, Massachusetts: Sinauer Associates. 1998
21.
go back to reference Koella JC, Lyimo EO: Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). Journal of Medical Entomology. 1996, 33: 261-264.CrossRefPubMed Koella JC, Lyimo EO: Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). Journal of Medical Entomology. 1996, 33: 261-264.CrossRefPubMed
22.
go back to reference Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, Meuwissen JH, Robert V: Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1994, 88: 121-125. 10.1016/0035-9203(94)90534-7.CrossRefPubMed Mulder B, Tchuinkam T, Dechering K, Verhave JP, Carnevale P, Meuwissen JH, Robert V: Malaria transmission-blocking activity in experimental infections of Anopheles gambiae from naturally infected Plasmodium falciparum gametocyte carriers. Trans R Soc Trop Med Hyg. 1994, 88: 121-125. 10.1016/0035-9203(94)90534-7.CrossRefPubMed
23.
go back to reference Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, Carnevale P, Meuwissen JH, Robert V: Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop Med Parasitol. 1993, 44: 271-276.PubMed Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, Carnevale P, Meuwissen JH, Robert V: Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop Med Parasitol. 1993, 44: 271-276.PubMed
24.
go back to reference Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119 ( Pt 2): 113-125. 10.1017/S0031182099004552.CrossRef Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119 ( Pt 2): 113-125. 10.1017/S0031182099004552.CrossRef
25.
go back to reference Su X, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed Su X, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed
26.
go back to reference Lyimo EO, Koella JC: Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology. 1992, 104 (Pt 2): 233-237.CrossRef Lyimo EO, Koella JC: Relationship between body size of adult Anopheles gambiae s.l. and infection with the malaria parasite Plasmodium falciparum. Parasitology. 1992, 104 (Pt 2): 233-237.CrossRef
27.
go back to reference Conway DJ, Greenwood BM, McBride JS: The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 1991, 103 Pt 1: 1-6.CrossRefPubMed Conway DJ, Greenwood BM, McBride JS: The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 1991, 103 Pt 1: 1-6.CrossRefPubMed
28.
go back to reference Magesa SM, Mdira KY, Babiker HA, Alifrangis M, Farnert A, Simonsen PE, Bygbjerg IC, Walliker D, Jakobsen PH: Diversity of Plasmodium falciparum clones infecting children living in a holoendemic area in north-eastern Tanzania. Acta Trop. 2002, 84: 83-92. 10.1016/S0001-706X(02)00179-1.CrossRefPubMed Magesa SM, Mdira KY, Babiker HA, Alifrangis M, Farnert A, Simonsen PE, Bygbjerg IC, Walliker D, Jakobsen PH: Diversity of Plasmodium falciparum clones infecting children living in a holoendemic area in north-eastern Tanzania. Acta Trop. 2002, 84: 83-92. 10.1016/S0001-706X(02)00179-1.CrossRefPubMed
29.
go back to reference Billingsley PF, Sinden RE: Determinants of Malaria-Mosquito Specificity. Parasitology Today. 1997, 13: 297-301. 10.1016/S0169-4758(97)01094-6.CrossRef Billingsley PF, Sinden RE: Determinants of Malaria-Mosquito Specificity. Parasitology Today. 1997, 13: 297-301. 10.1016/S0169-4758(97)01094-6.CrossRef
30.
go back to reference Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, Ansorge W, Kafatos FC, Collins FH: Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science. 1997, 276: 425-428. 10.1126/science.276.5311.425.CrossRefPubMed Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, Ansorge W, Kafatos FC, Collins FH: Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science. 1997, 276: 425-428. 10.1126/science.276.5311.425.CrossRefPubMed
31.
go back to reference Zheng L, Wang S, Romans P, Zhao H, Luna C, Benedict MQ: Quantitative trait loci in Anopheles gambiae controlling the encapsulation response against Plasmodium cynomolgi Ceylon. BMC Genet. 2003, 4: 16-10.1186/1471-2156-4-16.PubMedCentralCrossRefPubMed Zheng L, Wang S, Romans P, Zhao H, Luna C, Benedict MQ: Quantitative trait loci in Anopheles gambiae controlling the encapsulation response against Plasmodium cynomolgi Ceylon. BMC Genet. 2003, 4: 16-10.1186/1471-2156-4-16.PubMedCentralCrossRefPubMed
32.
go back to reference Taylor LH: Infection rates in, and the number of Plasmodium falciparum genotypes carried by Anopheles mosquitoes in Tanzania. Ann Trop Med Parasitol. 1999, 93: 659-662. 10.1080/00034989958168.CrossRefPubMed Taylor LH: Infection rates in, and the number of Plasmodium falciparum genotypes carried by Anopheles mosquitoes in Tanzania. Ann Trop Med Parasitol. 1999, 93: 659-662. 10.1080/00034989958168.CrossRefPubMed
33.
go back to reference Bonnet S, Gouagna LC, Paul RE, Safeukui I, Meunier JY, Boudin C: Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg. 2003, 97: 53-59. 10.1016/S0035-9203(03)90022-8.CrossRefPubMed Bonnet S, Gouagna LC, Paul RE, Safeukui I, Meunier JY, Boudin C: Estimation of malaria transmission from humans to mosquitoes in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Trans R Soc Trop Med Hyg. 2003, 97: 53-59. 10.1016/S0035-9203(03)90022-8.CrossRefPubMed
34.
go back to reference Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Verhave JP, Boudin C: The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: an estimation of parasite efficacy. Trop Med Int Health. 1998, 3: 21-28. 10.1046/j.1365-3156.1998.00156.x.CrossRefPubMed Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Verhave JP, Boudin C: The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: an estimation of parasite efficacy. Trop Med Int Health. 1998, 3: 21-28. 10.1046/j.1365-3156.1998.00156.x.CrossRefPubMed
35.
go back to reference Targett GA: Plasmodium falciparum: natural and experimental transmission-blocking immunity. Immunol Lett. 1988, 19: 235-240. 10.1016/0165-2478(88)90148-4.CrossRefPubMed Targett GA: Plasmodium falciparum: natural and experimental transmission-blocking immunity. Immunol Lett. 1988, 19: 235-240. 10.1016/0165-2478(88)90148-4.CrossRefPubMed
Metadata
Title
Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum
Authors
Louis Lambrechts
Jean Halbert
Patrick Durand
Louis C Gouagna
Jacob C Koella
Publication date
01-12-2005
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2005
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-4-3

Other articles of this Issue 1/2005

Malaria Journal 1/2005 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.