期刊论文详细信息
Particle and Fibre Toxicology
Larval nutrition differentially affects adult fitness and Plasmodium development in the malaria vectors Anopheles gambiae and Anopheles stephensi
Peter F Billingsley4  A Jenny Mordue-Luntz5  Margaret Brown2  Valerie Johnston5  Antoine J Vigneau3  Renate C Smallegange6  Willem Takken1 
[1] Laboratory of Entomology, Wageningen University, PO Box 8031, 6700, EH Wageningen, The Netherlands;Current address: School of Pharmacy, Robert Gordon University, Schoolhill, Aberdeen AB10 1FR, UK;Current address: 18 Jasmine Court, CB1 8BG Cambridge, UK;Current address: Sanaria Inc, 9800 Medical Center Drive, Rockville, MD 20850, USA;School of Biological Sciences, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland UK;Current address: Wageningen Academic Publishers, PO Box 220, 6700, AE Wageningen, The Netherlands
关键词: Fitness;    Body size;    Blood-feeding;    Plasmodium yoelii nigeriensis;    Mosquito;    Anopheles stephensi;    Anopheles gambiae sensu stricto;   
Others  :  823648
DOI  :  10.1186/1756-3305-6-345
 received in 2012-12-19, accepted in 2013-12-04,  发布年份 2013
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【 摘 要 】

Background

Mosquito fitness is determined largely by body size and nutritional reserves. Plasmodium infections in the mosquito and resultant transmission of malaria parasites might be compromised by the vector’s nutritional status. We studied the effects of nutritional stress and malaria parasite infections on transmission fitness of Anopheles mosquitoes.

Methods

Larvae of Anopheles gambiae sensu stricto and An. stephensi were reared at constant density but with nutritionally low and high diets. Fitness of adult mosquitoes resulting from each dietary class was assessed by measuring body size and lipid, protein and glycogen content. The size of the first blood meal was estimated by protein analysis. Mosquitoes of each dietary class were fed upon a Plasmodium yoelii nigeriensis-infected mouse, and parasite infections were determined 5 d after the infectious blood meal by dissection of the midguts and by counting oocysts. The impact of Plasmodium infections on gonotrophic development was established by dissection.

Results

Mosquitoes raised under low and high diets emerged as adults of different size classes comparable between An. gambiae and An. stephensi. In both species low-diet females contained less protein, lipid and glycogen upon emergence than high-diet mosquitoes. The quantity of larval diet impacted strongly upon adult blood feeding and reproductive success. The prevalence and intensity of P. yoelii nigeriensis infections were reduced in low-diet mosquitoes of both species, but P. yoelii nigeriensis impacted negatively only on low-diet, small-sized An. gambiae considering survival and egg maturation. There was no measurable fitness effect of P. yoelii nigeriensis on An. stephensi.

Conclusions

Under the experimental conditions, small-sized An. gambiae expressed high mortality, possibly caused by Plasmodium infections, the species showing distinct physiological concessions when nutrionally challenged in contrast to well-fed, larger siblings. Conversely, An. stephensi was a robust, successful vector regardless of its nutrional status upon emergence. The data suggest that small-sized An. gambiae, therefore, would contribute little to malaria transmission, whereas this size effect would not affect An. stephensi.

【 授权许可】

   
2013 Takken et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Briegel H: Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), Vectors of Malaria. J Med Entomol 1990, 27:839-850.
  • [2]Takken W, Klowden MJ, Chambers GM: Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): the disadvantage of being small. J Med Entomol 1998, 35:639-645.
  • [3]Ng’habi KR, Huho BJ, Nkwengulila G, Killeen GF, Knols BGJ, Ferguson HM: Sexual selection in mosquito swarms: may the best man lose? Anim Behav 2008, 76:105-112.
  • [4]Hurd H: Interactions between parasites and insects vectors. Mem Inst Oswaldo Cruz 1994, 89(Suppl 2):27-30.
  • [5]Gillies MT: The recognition of age-groups within populations of Anopheles gambiae by the pre-gravid rate and the sporozoite rate. Ann Trop Med Parasitol 1954, 48:58-74.
  • [6]Gillies MT: The pre-gravid phase of ovarian development in Anopheles funestus. Ann Trop Med Parasit 1955, 49:320-325.
  • [7]Hurd H: Manipulation of medically important insect vectors by their parasites. Annu Rev Entomol 2003, 48:141-161.
  • [8]Rivero A, Ferguson HM: The energetic budget of Anopheles stephensi infected with Plasmodium chabaudi: is energy depletion a mechanism for virulence? Proc R Soc Lond Ser B-Biol Sci 2003, 270:1365-1371.
  • [9]Dawes EJ, Churcher TS, Zhuang S, Sinden RE, Basáñez MF: Anopheles mortality is both age- and Plasmodium-density dependent: implications for malaria transmission. Malar J 2009, 8:228. BioMed Central Full Text
  • [10]Hurd H, Hogg JC, Renshaw M: Interactions between bloodfeeding, fecundity and infection in mosquitoes. Parasitol Today 1995, 11:411-416.
  • [11]Hogg JC, Carwardine S, Hurd H: The effect of Plasmodium yoelii nigeriensis infection on ovarian protein accumulation by Anopheles stephensi. Parasitol Res 1997, 83:374-379.
  • [12]Lyimo EO, Takken W: Effects of adult body size on fecundity and the pregravid rate of Anopheles gambiae females in Tanzania. Med Vet Entomol 1993, 7:328-332.
  • [13]Okech BA, Gouagna LC, Yan G, Githure JI, Beier JC: Larval habitats of Anopheles gambiae s.s. (Diptera: Culicidae) influences vector competence to Plasmodium falciparum parasites. Malar J 2007, 6:50. BioMed Central Full Text
  • [14]Van Händel E: Rapid determination of glycogen and sugars in mosquitoes. J Am Mosq Control Assoc 1985, 1:299-301.
  • [15]Van Händel E: Rapid determination of total lipids in mosquitoes. J Am Mosq Control Assoc 1985, 1:302-304.
  • [16]Billingsley PF, Hecker H: Blood digestion in the mosquito, Anopheles stephensi Liston (Diptera: Culicidae): activity and distribution of trypsin, aminopeptidase, and alpha-glucosidase in the midgut. J Med Entomol 1991, 28:865-871.
  • [17]Billingsley PF, Hodivala KJ, Winger LA, Sinden RE: Detection of mature malaria infections in live mosquitoes. Trans R Soc Trop Med Hyg 1991, 85:450-453.
  • [18]Sokal RR, Rohlf FJ: Biometry: the Principles and the Practice of Statistics in Biological Research. 3rd edition. New York: WH Freeman and Company; 1998.
  • [19]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.
  • [20]Billingsley PF, Medley GF, Charlwood D, Sinden RE: Relationship between prevalence and intensity of Plasmodium falciparum infection in natural populations of Anopheles mosquitos. Am J Trop Med Hyg 1994, 51:260-270.
  • [21]Christophers SR: The development of the egg follicle in anophelines. Paludism 1911, 2:73-78.
  • [22]Oude Voshaar JH: Statistiek voor Onderzoekers. Met voorbeelden uit de Landbouw en Milieuwetenschappen. The Netherlands: Wageningen Pers, Wageningen; 1994.
  • [23]Medley GF, Sinden RE, Fleck S, Billingsley PF, Tirawanchai N, Rodriguez MH: Heterogeneity in patterns of malarial oocyst infections in the mosquito vector. Parasitology 1993, 106:441-449.
  • [24]Foster WA, Takken W: Nectar-related vs. human-related volatiles: behavioural response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding. Bull Entomol Res 2004, 94:145-157.
  • [25]Koenraadt CJM, Takken W: Cannibalism and predation among larvae of the Anopheles gambiae complex. Med Vet Entomol 2003, 17:61-66.
  • [26]Lyimo EO, Takken W, Koella JC: Effect of rearing temperature and larval density on larval survival, age at pupation and adult size of Anopheles gambiae. Entomol Exp Appl 1992, 63:265-271.
  • [27]Steinwascher K: Relationship between pupal mass and adult survivorship and fecundity for Aedes aegypti. Environ Entomol 1982, 11:150-153.
  • [28]Packer MJ, Corbet P: Size variation and reproductive success of female Aedes punctor (Diptera: Culicidae). Ecol Entomol 1989, 14:297-309.
  • [29]Charlwood JD, Smith T, Billingsley FF, Takken W, Lyimo EOK, Meuwissen JHET: Survival and infection probabilities of anthropophagie anophelines from an area of high prevalence of Plasmodium falciparum in humans. Bull Entomol Res 1997, 87:445-453.
  • [30]Briegel H: Physiological bases of mosquito ecology. J Vector Ecol 2003, 28:1-11.
  • [31]Harrington LC, Edman JD, Scott TW: Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 2001, 38:411-422.
  • [32]Okanda FM, Dao A, Njiru BN, Arija J, Akelo HA, Toure Y, Odulaja A, Beier JC, Githure JI, Yan G, et al.: Behavioural determinants of gene flow in malaria vector populations: Anopheles gambiae males select large females as mates. Malar J 2002, 1:10. BioMed Central Full Text
  • [33]Ponlawat A, Harrington LC: Factors associated with male mating success of the dengue vector mosquito, Aedes aegypti. Am J Trop Med Hyg 2009, 80:395-400.
  • [34]Pichon G, Awono-Ambene HP, Robert V: High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host. Parasitology 2000, 121:115-120.
  • [35]Lyimo EO, Koella JC: Relationship between body size of adult Anopheles gambiae s.l. and infection with malaria parasite Plasmodium falciparum. Parasitology 1992, 104:233-237.
  • [36]Barillas Mury C, Kumar S: Plasmodium-mosquito interactions: a tale of dangerous liaisons. Cell Microbiol 2005, 7:1539-1545.
  • [37]Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, et al.: 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 Parasit 2003, 33:933-943.
  • [38]Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, Fowler K, Billker O, Franke-Fayard B, Janse CJ, Waters A, et al.: Corrigendum to: 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 (vol 33, pg 933, 2003). Int J Parasit 2004, 34:245-247.
  • [39]Cirimotich CM, Dong Y, Garver LS, Sim S, Dimopoulos G: Mosquito immune defenses against Plasmodium infection. Dev Comp Immunol 2010, 34:387-395.
  • [40]Dimopoulos G, Muller HM, Levashina EA, Kafatos FC: Innate immune defense against malaria infection in the mosquito. Curr Opin Immunol 2001, 13:79-88.
  • [41]Mendes AM, Schlegelmilch T, Cohuet A, Awono-Ambene P, De Iorio M, Fontenille D, Morlais I, Christophides GK, Kafatos FC, Vlachou D: Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa. PLoS Path 2008, 4:e1000069.
  • [42]Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G, et al.: Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
  • [43]Drexler AL, Vodovotz Y, Luckhart S: Plasmodium development in the mosquito: biology bottlenecks and opportunities for mathematical modeling. Trends Parasitol 2008, 24:333-336.
  • [44]Lambrechts L, Chavatte JM, Snounou G, Koella JC: Environmental influence on the genetic basis of mosquito resistance to malaria parasites. P Roy Soc B-Biol Sci 2006, 273:1501-1506.
  • [45]Yaro AS, Toure AM, Guindo A, Coulibaly MB, Dao A, Diallo M, Traore SF: Reproductive success in Anopheles arabiensis and the M and S molecular forms of Anopheles gambiae: do natural sporozoite infection and body size matter? Acta Trop 2012, 122:87-93.
  • [46]Ahmed AM, Maingon RD, Taylor PJ, Hurd H: The effects of infection with Plasmodium yoelii nigeriensis on the reproductive fitness of the mosquito Anopheles gambiae. Invertebr Reprod Dev 1999, 36:217-222.
  • [47]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.
  • [48]Pringle G: A quantitative study of naturally-acquired malaria infections in Anopheles gambiae and Anopheles funestus in a highly malarious area of East Africa. Trans R Soc Trop Med Hyg 1966, 60:626-632.
  • [49]Haji H, Smith T, Charlwood JD, Meuwissen JH: Absence of relationships between selected human factors and natural infectivity of Plasmodium falciparum to mosquitoes in an area of high transmission. Parasitology 1996, 113:425-431.
  • [50]Hopwood JA, Ahmed AM, Polwart A, Williams GT, Hurd H: Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. J Exp Biol 2001, 204:2773-2780.
  • [51]Ferguson HM, Read AF: Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 2002, 18:256-260.
  • [52]Straif SC, Beier JC: Effects of sugar availability on the blood-feeding behavior of Anopheles gambiae (Diptera: Culicidae). J Med Entomol 1996, 33:608-612.
  • [53]Okech BA, Gouagna LC, Killeen GF, Knols BG, Kabiru EW, Beier JC, Yan G, Githure JI: Influence of sugar availability and indoor microclimate on survival of Anopheles gambiae (Diptera: Culicidae) under semifield conditions in western Kenya. J Med Entomol 2003, 40:657-663.
  • [54]Anderson RA, Knols BG, Koella JC: Plasmodium falciparum sporozoites increase feeding-associated mortality of their mosquito hosts Anopheles gambiae s.l. Parasitology 2000, 120:329-333.
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