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Published in: Malaria Journal 1/2008

Open Access 01-12-2008 | Research

Comparison of male reproductive success in malaria-refractory and susceptible strains of Anopheles gambiae

Authors: Maarten J Voordouw, Jacob C Koella, Hilary Hurd

Published in: Malaria Journal | Issue 1/2008

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Abstract

Background

In female mosquitoes that transmit malaria, the benefits of being refractory to the Plasmodium parasite are balanced by the immunity costs in the absence of infection. Male mosquitoes, however, gain no advantage from being refractory to blood-transmitted parasites, so that any costs associated with an enhanced immune system in the males limit the evolution of female refractoriness and has practical implications for the release of transgenic males.

Methods

Aspects of the male cost of carrying Plasmodium-refractory genes were estimated by comparing the males' immune response and reproductive success among strains of Anopheles gambiae that had been selected for refractoriness or extreme susceptibility to the rodent malaria parasite, Plasmodium yoelii nigeriensis. The refractory males had a stronger melanization response than males from the susceptible line. Four traits were used as correlates of a male's reproductive success: the proportion of females that were inseminated by a fixed number of males in a cage within a fixed time frame, the proportion of females with motile sperm in their spermathecae, the proportion of ovipositing females, and the mean number of eggs per batch.

Results

Although there were significant differences among groups of males in sperm motility and oviposition success, these differences in male reproductive success were not associated with the refractory or susceptible male genotypes. Contrary to expectation, females mated to early emerging refractory males laid significantly more eggs per batch than females mated to later emerging susceptible males. Sperm motility and oviposition success were strongly correlated suggesting that variation in sperm motility influences female oviposition and ultimately male reproductive success.

Conclusion

An increased melanization response in male A. gambiae does not diminish male reproductive success under the experimental protocol used in this study. That refractory males induced ovipositing females to lay more eggs than susceptible males is an interesting result for any strategy considering the release of transgenic males. That sperm motility influences female oviposition is also important for the release of transgenic males.
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Literature
1.
go back to reference Sheldon BC, Verhulst S: Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996, 11: 317-321. 10.1016/0169-5347(96)10039-2.CrossRefPubMed Sheldon BC, Verhulst S: Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996, 11: 317-321. 10.1016/0169-5347(96)10039-2.CrossRefPubMed
2.
go back to reference Kraaijeveld AR, Godfray HCJ: Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature. 1997, 389: 278-280. 10.1038/38483.CrossRefPubMed Kraaijeveld AR, Godfray HCJ: Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature. 1997, 389: 278-280. 10.1038/38483.CrossRefPubMed
3.
go back to reference Koella JC, Boete C: A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution. 2002, 56: 1074-1079.CrossRefPubMed Koella JC, Boete C: A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution. 2002, 56: 1074-1079.CrossRefPubMed
4.
go back to reference Stearns SC: The evolution of life-histories. 1992, Oxford: Oxford University Press Stearns SC: The evolution of life-histories. 1992, Oxford: Oxford University Press
5.
go back to reference Hogg JC, Cawardine S, Hurd H: The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitol Res. 1997, 83: 374-379. 10.1007/s004360050265.CrossRefPubMed Hogg JC, Cawardine S, Hurd H: The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitol Res. 1997, 83: 374-379. 10.1007/s004360050265.CrossRefPubMed
6.
go back to reference Hogg JC, Hurd H: Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol. 1995, 9: 176-180. 10.1111/j.1365-2915.1995.tb00175.x.CrossRefPubMed Hogg JC, Hurd H: Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol. 1995, 9: 176-180. 10.1111/j.1365-2915.1995.tb00175.x.CrossRefPubMed
7.
go back to reference Hogg JC, Hurd H: Plasmodium yoelii nigeriensis : The effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology. 1995, 111: 555-562.CrossRefPubMed Hogg JC, Hurd H: Plasmodium yoelii nigeriensis : The effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology. 1995, 111: 555-562.CrossRefPubMed
8.
go back to reference Anderson RA, Knols BGJ, Koella JC: Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology. 2000, 120: 329-333. 10.1017/S0031182099005570.CrossRefPubMed Anderson RA, Knols BGJ, Koella JC: Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology. 2000, 120: 329-333. 10.1017/S0031182099005570.CrossRefPubMed
9.
go back to reference Ferguson HM, Read AF: Why is the effect of malaria parasites on mosquito survival still unresolved?. Trends Parasitol. 2002, 18: 256-261. 10.1016/S1471-4922(02)02281-X.CrossRefPubMed Ferguson HM, Read AF: Why is the effect of malaria parasites on mosquito survival still unresolved?. Trends Parasitol. 2002, 18: 256-261. 10.1016/S1471-4922(02)02281-X.CrossRefPubMed
10.
go back to reference Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, Sinden RE: The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol. 2003, 33: 933-943. 10.1016/S0020-7519(03)00112-7.CrossRefPubMed Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, Sinden RE: The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol. 2003, 33: 933-943. 10.1016/S0020-7519(03)00112-7.CrossRefPubMed
11.
go back to reference Sinden RE, Alavi Y, Raine JD: Mosquito-malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness. Insect Biochem Mol Biol. 2004, 34: 625-629. 10.1016/j.ibmb.2004.03.015.CrossRefPubMed Sinden RE, Alavi Y, Raine JD: Mosquito-malaria interactions: a reappraisal of the concepts of susceptibility and refractoriness. Insect Biochem Mol Biol. 2004, 34: 625-629. 10.1016/j.ibmb.2004.03.015.CrossRefPubMed
12.
go back to reference Vaughan JA, Hensley L, Beier JC: Sporogonic development of Plasmodium yoelii in five anopheline species. J Parasitol. 1994, 80: 674-681. 10.2307/3283245.CrossRefPubMed Vaughan JA, Hensley L, Beier JC: Sporogonic development of Plasmodium yoelii in five anopheline species. J Parasitol. 1994, 80: 674-681. 10.2307/3283245.CrossRefPubMed
13.
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. 10.1126/science.3532325.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. 10.1126/science.3532325.CrossRefPubMed
14.
go back to reference Hurd H, Taylor PJ, Adams D, Underhill A, Eggleston P: Evaluating the costs of mosquito resistance to malaria parasites. Evolution. 2005, 59: 2560-2572.PubMedCentralCrossRefPubMed Hurd H, Taylor PJ, Adams D, Underhill A, Eggleston P: Evaluating the costs of mosquito resistance to malaria parasites. Evolution. 2005, 59: 2560-2572.PubMedCentralCrossRefPubMed
15.
go back to reference Niare O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang J, 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.CrossRef Niare O, Markianos K, Volz J, Oduol F, Toure A, Bagayoko M, Sangare D, Traore SF, Wang J, 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.CrossRef
16.
go back to reference Riehle MM, Markianos K, Lambrechts L, Xia A, Sharakhov I, Koella JC, Vernick KD: A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae. Malaria Journal. 2007, 6: 87-10.1186/1475-2875-6-87.PubMedCentralCrossRefPubMed Riehle MM, Markianos K, Lambrechts L, Xia A, Sharakhov I, Koella JC, Vernick KD: A major genetic locus controlling natural Plasmodium falciparum infection is shared by East and West African Anopheles gambiae. Malaria Journal. 2007, 6: 87-10.1186/1475-2875-6-87.PubMedCentralCrossRefPubMed
17.
go back to reference Riehle MM, Markianos K, Niare O, Xu J, Li J, Toure AM, Podiougou B, Oduol F, Diawara S, Diallo M, Coulibaly B, Ouatara A, Kruglyak L, Traore SF, Vernick KD: Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science. 2006, 312: 577-579. 10.1126/science.1124153.CrossRefPubMed Riehle MM, Markianos K, Niare O, Xu J, Li J, Toure AM, Podiougou B, Oduol F, Diawara S, Diallo M, Coulibaly B, Ouatara A, Kruglyak L, Traore SF, Vernick KD: Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science. 2006, 312: 577-579. 10.1126/science.1124153.CrossRefPubMed
18.
go back to reference Yan G, Severson DW, Christensen BM: Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution. 1997, 51: 441-450. 10.2307/2411116.CrossRef Yan G, Severson DW, Christensen BM: Costs and benefits of mosquito refractoriness to malaria parasites: implications for genetic variability of mosquitoes and genetic control of malaria. Evolution. 1997, 51: 441-450. 10.2307/2411116.CrossRef
19.
go back to reference Rice WR: Sexually antagonistic genes: experimental evidence. Science. 1992, 256: 1436-1439. 10.1126/science.1604317.CrossRefPubMed Rice WR: Sexually antagonistic genes: experimental evidence. Science. 1992, 256: 1436-1439. 10.1126/science.1604317.CrossRefPubMed
20.
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 A, 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 A, Collins FH: Malaria control with genetically manipulated insect vectors. Science. 2002, 298: 119-121. 10.1126/science.1078278.CrossRefPubMed
21.
go back to reference Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, Miller LH: Plasmodium gallinaceum : a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol. 1995, 80: 583-595. 10.1006/expr.1995.1074.CrossRefPubMed Vernick KD, Fujioka H, Seeley DC, Tandler B, Aikawa M, Miller LH: Plasmodium gallinaceum : a refractory mechanism of ookinete killing in the mosquito, Anopheles gambiae. Exp Parasitol. 1995, 80: 583-595. 10.1006/expr.1995.1074.CrossRefPubMed
22.
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.CrossRef 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.CrossRef
23.
go back to reference Christensen BM, Li J, Chen CC, Nappi AJ: Melanization immune responses in mosquito vectors. Trends Parasitol. 2005, 21: 192-199. 10.1016/j.pt.2005.02.007.CrossRefPubMed Christensen BM, Li J, Chen CC, Nappi AJ: Melanization immune responses in mosquito vectors. Trends Parasitol. 2005, 21: 192-199. 10.1016/j.pt.2005.02.007.CrossRefPubMed
24.
go back to reference Paskewitz S, Riehle M: Response of Plasmodium refractory and susceptible strains of Anopheles gambiae to innoculated Sephadex beads. Dev Comp Immunol. 1994, 18: 369-375. 10.1016/0145-305X(94)90002-7.CrossRef Paskewitz S, Riehle M: Response of Plasmodium refractory and susceptible strains of Anopheles gambiae to innoculated Sephadex beads. Dev Comp Immunol. 1994, 18: 369-375. 10.1016/0145-305X(94)90002-7.CrossRef
25.
go back to reference Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C, do Rosario VE: The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera : Culicidae) from Sao Tome Island. J Vector Ecol. 2002, 27: 178-183.PubMed Charlwood JD, Pinto J, Sousa CA, Madsen H, Ferreira C, do Rosario VE: The swarming and mating behaviour of Anopheles gambiae s.s. (Diptera : Culicidae) from Sao Tome Island. J Vector Ecol. 2002, 27: 178-183.PubMed
26.
go back to reference Charlwood JD, Thompson R, Madsen H: Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malaria Journal. 2003, 2: Charlwood JD, Thompson R, Madsen H: Observations on the swarming and mating behaviour of Anopheles funestus from southern Mozambique. Malaria Journal. 2003, 2:
27.
go back to reference Yuval B: Mating systems of blood-feeding flies. Annu Rev Entomol. 2006, 51: 413-440. 10.1146/annurev.ento.51.110104.151058.CrossRefPubMed Yuval B: Mating systems of blood-feeding flies. Annu Rev Entomol. 2006, 51: 413-440. 10.1146/annurev.ento.51.110104.151058.CrossRefPubMed
28.
go back to reference Tripet F, Toure YT, Dolo G, Lanzaro GC: Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg. 2003, 68: 1-5.PubMed Tripet F, Toure YT, Dolo G, Lanzaro GC: Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg. 2003, 68: 1-5.PubMed
29.
go back to reference Parker GA: Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc. 1970, 45: 525-567. 10.1111/j.1469-185X.1970.tb01176.x.CrossRef Parker GA: Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc. 1970, 45: 525-567. 10.1111/j.1469-185X.1970.tb01176.x.CrossRef
30.
go back to reference Suleman M: Intraspecific variation in the reproductive capacity of Anopheles stephensi (Diptera, Culicidae). J Med Entomol. 1990, 27: 819-828.CrossRefPubMed Suleman M: Intraspecific variation in the reproductive capacity of Anopheles stephensi (Diptera, Culicidae). J Med Entomol. 1990, 27: 819-828.CrossRefPubMed
31.
go back to reference Yuval B, Bouskila A: Temporal dynamics of mating and predation in mosquito swarms. Oecologia. 1993, 95: 65-69.CrossRef Yuval B, Bouskila A: Temporal dynamics of mating and predation in mosquito swarms. Oecologia. 1993, 95: 65-69.CrossRef
32.
go back to reference Yuval B, Wekesa JW, Washino RK: Effect of body size on swarming behavior and mating success of male Anopheles freeborni (Diptera: Culicidae). J Insect Physiol. 1993, 6: 333-342. Yuval B, Wekesa JW, Washino RK: Effect of body size on swarming behavior and mating success of male Anopheles freeborni (Diptera: Culicidae). J Insect Physiol. 1993, 6: 333-342.
33.
go back to reference Bock ME, Reisen WK, Milby MM: Lifetime mating pattern of laboratory-adapted Culex tarsalis males. Mosq News. 1983, 43: 350-354. Bock ME, Reisen WK, Milby MM: Lifetime mating pattern of laboratory-adapted Culex tarsalis males. Mosq News. 1983, 43: 350-354.
34.
go back to reference Mahmood F, Reisen WK: Anopheles stephensi (Diptera: Culicidae): changes in male mating competence and reproductive system morphology associated with aging and mating. J Med Entomol. 1982, 19: 573-588.CrossRefPubMed Mahmood F, Reisen WK: Anopheles stephensi (Diptera: Culicidae): changes in male mating competence and reproductive system morphology associated with aging and mating. J Med Entomol. 1982, 19: 573-588.CrossRefPubMed
35.
go back to reference Okanda FM, Dao A, Njiru BN, Arija J, Akelo HA, Toure Y, Odulaja A, Beier JC, Githure JI, Yan G, Gouagna LC, Knols BGJ, Killeen GF: Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malaria Journal. 2002, 1: 1-7. 10.1186/1475-2875-1-10.CrossRef Okanda FM, Dao A, Njiru BN, Arija J, Akelo HA, Toure Y, Odulaja A, Beier JC, Githure JI, Yan G, Gouagna LC, Knols BGJ, Killeen GF: Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malaria Journal. 2002, 1: 1-7. 10.1186/1475-2875-1-10.CrossRef
36.
go back to reference Charlwood JD, Jones MDR: Mating behaviour in the mosquito, Anopheles gambiae s.l. I. Close range and contact behaviour. Physiol Entomol. 1979, 4: 111-120. 10.1111/j.1365-3032.1979.tb00185.x.CrossRef Charlwood JD, Jones MDR: Mating behaviour in the mosquito, Anopheles gambiae s.l. I. Close range and contact behaviour. Physiol Entomol. 1979, 4: 111-120. 10.1111/j.1365-3032.1979.tb00185.x.CrossRef
37.
go back to reference Verhoek BA, Takken W: Age effects on the Insemination rate of Anopheles gambiae sl in the laboratory. Entomol Exp Appl. 1994, 72: 167-172. 10.1007/BF02383551.CrossRef Verhoek BA, Takken W: Age effects on the Insemination rate of Anopheles gambiae sl in the laboratory. Entomol Exp Appl. 1994, 72: 167-172. 10.1007/BF02383551.CrossRef
38.
go back to reference Ng'habi KR, John B, Nkwengulila G, Knols BGJ, Killeen GF, Ferguson HM: Effect of larval crowding on mating competitiveness of Anopheles gambiae mosquitoes. Malaria Journal. 2005, 4: 1-9. 10.1186/1475-2875-4-49.CrossRef Ng'habi KR, John B, Nkwengulila G, Knols BGJ, Killeen GF, Ferguson HM: Effect of larval crowding on mating competitiveness of Anopheles gambiae mosquitoes. Malaria Journal. 2005, 4: 1-9. 10.1186/1475-2875-4-49.CrossRef
39.
go back to reference Mahmood F, Reisen WK: Anopheles culicifacies : effects of age on the male reproductive system and mating ability of virgin adult mosquitoes. Med Vet Entomol. 1994, 8: 31-37. 10.1111/j.1365-2915.1994.tb00380.x.CrossRefPubMed Mahmood F, Reisen WK: Anopheles culicifacies : effects of age on the male reproductive system and mating ability of virgin adult mosquitoes. Med Vet Entomol. 1994, 8: 31-37. 10.1111/j.1365-2915.1994.tb00380.x.CrossRefPubMed
40.
go back to reference Bryan JH: Results of consecutive matings of female Anopheles gambiae species B with fertile and sterile males. Nature. 1968, 218: 489-10.1038/218489a0.CrossRefPubMed Bryan JH: Results of consecutive matings of female Anopheles gambiae species B with fertile and sterile males. Nature. 1968, 218: 489-10.1038/218489a0.CrossRefPubMed
41.
go back to reference Bryan JH: Further studies on consecutive matings in the Anopheles gambiae complex. Nature. 1972, 239: 519-520. 10.1038/239519a0.CrossRef Bryan JH: Further studies on consecutive matings in the Anopheles gambiae complex. Nature. 1972, 239: 519-520. 10.1038/239519a0.CrossRef
42.
go back to reference Klowden MJ: Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J Insect Physiol. 2001, 47: 661-666. 10.1016/S0022-1910(00)00127-X.CrossRefPubMed Klowden MJ: Sexual receptivity in Anopheles gambiae mosquitoes: absence of control by male accessory gland substances. J Insect Physiol. 2001, 47: 661-666. 10.1016/S0022-1910(00)00127-X.CrossRefPubMed
43.
go back to reference Klowden MJ: Switchover to the mated state by spermathecal activation in female Anopheles gambiae mosquitoes. J Insect Physiol. 2006, 52: 679-684. 10.1016/j.jinsphys.2006.03.006.CrossRefPubMed Klowden MJ: Switchover to the mated state by spermathecal activation in female Anopheles gambiae mosquitoes. J Insect Physiol. 2006, 52: 679-684. 10.1016/j.jinsphys.2006.03.006.CrossRefPubMed
44.
go back to reference Marina CF, Ibarra JE, Arredondo-Jimenez JI, Fernandez-Salas I, Liedo P, Williams T: Adverse effects of covert iridovirus infection on life history and demographic parameters of Aedes aegypti. Entomol Exp Appl. 2003, 106: 53-61. 10.1046/j.1570-7458.2003.00010.x.CrossRef Marina CF, Ibarra JE, Arredondo-Jimenez JI, Fernandez-Salas I, Liedo P, Williams T: Adverse effects of covert iridovirus infection on life history and demographic parameters of Aedes aegypti. Entomol Exp Appl. 2003, 106: 53-61. 10.1046/j.1570-7458.2003.00010.x.CrossRef
45.
go back to reference Voordouw MJ, Koella JC: Genetic variation of male reproductive success in a laboratory population of Anopheles gambiae. Malaria Journal. 2007, 6: 1-11. 10.1186/1475-2875-6-99.CrossRef Voordouw MJ, Koella JC: Genetic variation of male reproductive success in a laboratory population of Anopheles gambiae. Malaria Journal. 2007, 6: 1-11. 10.1186/1475-2875-6-99.CrossRef
46.
go back to reference Grech K, Maung LA, Read AF: The effect of parental rearing conditions on offspring life history in Anopheles stephensi. Malaria Journal. 2007, 6: 1-9. 10.1186/1475-2875-6-130.CrossRef Grech K, Maung LA, Read AF: The effect of parental rearing conditions on offspring life history in Anopheles stephensi. Malaria Journal. 2007, 6: 1-9. 10.1186/1475-2875-6-130.CrossRef
47.
go back to reference Werner M, Simmons LW: Insect sperm motility. Biol Rev (Camb). 2008, 83: 191-208. 10.1111/j.1469-185X.2008.00039.x.CrossRef Werner M, Simmons LW: Insect sperm motility. Biol Rev (Camb). 2008, 83: 191-208. 10.1111/j.1469-185X.2008.00039.x.CrossRef
48.
go back to reference Snook RR: Sperm in competition: not playing by the numbers. Trends Ecol Evol. 2004, 20: 46-53. 10.1016/j.tree.2004.10.011.CrossRefPubMed Snook RR: Sperm in competition: not playing by the numbers. Trends Ecol Evol. 2004, 20: 46-53. 10.1016/j.tree.2004.10.011.CrossRefPubMed
49.
go back to reference Bernasconi G, Hellriegel B, Heyland A, Ward PI: Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L.). J Insect Physiol. 2002, 48: 197-203. 10.1016/S0022-1910(01)00164-0.CrossRefPubMed Bernasconi G, Hellriegel B, Heyland A, Ward PI: Sperm survival in the female reproductive tract in the fly Scathophaga stercoraria (L.). J Insect Physiol. 2002, 48: 197-203. 10.1016/S0022-1910(01)00164-0.CrossRefPubMed
50.
go back to reference Ward PI: Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). Journal of Zoology. 2000, 251: 349-353. 10.1111/j.1469-7998.2000.tb01085.x.CrossRef Ward PI: Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). Journal of Zoology. 2000, 251: 349-353. 10.1111/j.1469-7998.2000.tb01085.x.CrossRef
51.
go back to reference Klowden MJ, Chambers GM: Production of polymorphic sperm by anopheline mosquitoes and their fate within the female genital tract. J Insect Physiol. 2004, 50: 1163-1170. 10.1016/j.jinsphys.2004.10.008.CrossRefPubMed Klowden MJ, Chambers GM: Production of polymorphic sperm by anopheline mosquitoes and their fate within the female genital tract. J Insect Physiol. 2004, 50: 1163-1170. 10.1016/j.jinsphys.2004.10.008.CrossRefPubMed
52.
go back to reference Snook RR, Markow TA, Karr TL: Functional nonequivalence of sperm in Drosophila pseudoobscura. Proc Natl Acad Sci USA. 1994, 91: 11222-11226. 10.1073/pnas.91.23.11222.PubMedCentralCrossRefPubMed Snook RR, Markow TA, Karr TL: Functional nonequivalence of sperm in Drosophila pseudoobscura. Proc Natl Acad Sci USA. 1994, 91: 11222-11226. 10.1073/pnas.91.23.11222.PubMedCentralCrossRefPubMed
53.
go back to reference Neems RM, McLachlan AJ, Chambers R: Body size and lifetime mating success of male midges (Diptera: Chironomidae). Anim Behav. 1990, 40: 648-652. 10.1016/S0003-3472(05)80694-3.CrossRef Neems RM, McLachlan AJ, Chambers R: Body size and lifetime mating success of male midges (Diptera: Chironomidae). Anim Behav. 1990, 40: 648-652. 10.1016/S0003-3472(05)80694-3.CrossRef
54.
go back to reference Chambers GM, Klowden MJ: Age of Anopheles gambiae Giles male mosquitoes at time of mating influences female oviposition. J Vector Ecol. 2001, 26: 196-201.PubMed Chambers GM, Klowden MJ: Age of Anopheles gambiae Giles male mosquitoes at time of mating influences female oviposition. J Vector Ecol. 2001, 26: 196-201.PubMed
Metadata
Title
Comparison of male reproductive success in malaria-refractory and susceptible strains of Anopheles gambiae
Authors
Maarten J Voordouw
Jacob C Koella
Hilary Hurd
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2008
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-7-103

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