Identification of morphological and chemical markers of dry- and wet-season conditions in female Anopheles gambiae mosquitoes

Particle and Fibre Toxicology

Gideon Wasserberg³  Nadja B Cech²  Brandie M Ehrmann²  Diana L Huestis¹  Tovi Lehmann¹  Kaira M Wagoner³ 

[1] Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, 12735 Twinbrook Parkway, Rockville, MD 20852, USA;Department of Chemistry and Biochemistry, University of North Carolina Greensboro, 435 Sullivan Bldg, Greensboro, NC 27402, USA;Department of Biology, University of North Carolina Greensboro, 235 Eberhart Bldg, Greensboro, NC 27402, USA

关键词: Malaria;    Wing length;    Spiracle;    Photoperiod;    Cuticular hydrocarbon;    Aestivation;   

Others  :  1183575
DOI  :  10.1186/1756-3305-7-294

 received in 2014-02-10, accepted in 2014-06-11,  发布年份 2014

【 摘 要 】

Background

Increased understanding of the dry-season survival mechanisms of Anopheles gambiae in semi-arid regions could benefit vector control efforts by identifying weak links in the transmission cycle of malaria. In this study, we examined the effect of photoperiod and relative humidity on morphologic and chemical traits known to control water loss in mosquitoes.

Methods

Anopheles gambiae body size (indexed by wing length), mesothoracic spiracle size, and cuticular hydrocarbon composition (both standardized by body size) were examined in mosquitoes raised from eggs exposed to short photoperiod and low relative humidity, simulating the dry season, or long photoperiod and high relative humidity, simulating the wet-season.

Results

Mosquitoes exposed to short photoperiod exhibited larger body size and larger mesothoracic spiracle length than mosquitoes exposed to long photoperiod. Mosquitoes exposed to short photoperiod and low relative humidity exhibited greater total cuticular hydrocarbon amount than mosquitoes exposed to long photoperiod and high relative humidity. In addition, total cuticular hydrocarbon amount increased with age and was higher in mated females. Mean n-alkane retention time (a measure of cuticular hydrocarbon chain length) was lower in mosquitoes exposed to short photoperiod and low relative humidity, and increased with age. Individual cuticular hydrocarbon peaks were examined, and several cuticular hydrocarbons were identified as potential biomarkers of dry- and wet-season conditions, age, and insemination status.

Conclusions

Results from this study indicate that morphological and chemical changes underlie aestivation of Anopheles gambiae and may serve as biomarkers of aestivation.

【 授权许可】

   
2014 Wagoner et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

【 参考文献 】

• [1]World malaria report 2012. Geneva: World Health Organization; 2012. http://www.who.int/malaria/publications/world_malaria_report_2012/en/ webcite
• [2]World malaria report 2008. Geneva: World Health Organization; 2008. http://www.who.int/malaria/publications/atoz/9789241563697/en/ webcite
• [3]Collins FH, Kamau L, Ranson HA, Vulule JM: Molecular entomology and prospects for malaria control. Bull Wld Hlth Org 2000, 78(12):1412-1423.
• [4]Craig M, Snow R, Le Sueur D: A climate-based distribution model of malaria transmission in sub-Saharan Africa. Trends Parasitol 1999, 15(3):105-111.
• [5]Sogoba N, Doumbia S, Vounatsou P, Baber I, Keita M, Maiga M, Traoré SF, Touré A, Dolo G, Smith T: Monitoring of larval habitats and mosquito densities in the Sudan savanna of Mali: implications for malaria vector control. Am J Trop Med Hyg 2007, 77(1):82-88.
• [6]Adamou A, Dao A, Timbine S, Kassogué Y, Yaro AS, Diallo M, Traoré SF, Huestis DL, Lehmann T: The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar J 2011, 10:151. BioMed Central Full Text
• [7]Lehmann FO, Dao A, Adamou A, Kassogue Y, Diallo M, Sékou T, Coscaron-Arias C: Aestivation of the African malaria mosquito, Anopheles gambiae in the Sahel. Am J Trop Med Hyg 2010, 83(3):601-606.
• [8]Beier J, Copeland R, Oyaro C, Masinya A, Odago W, Oduor S, Koech D, Roberts C: Anopheles gambiae complex egg-stage survival in dry soil from larval development sites in western Kenya. J Am Mosquito Contr 1990, 6(1):105.
• [9]Minakawa N, Githure J, Beier J, Yan G: Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol 2001, 38(3):388-392.
• [10]Koenraadt C, Paaijmans K, Githeko A, Knols B, Takken W: Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar J 2003, 2(1):20. BioMed Central Full Text
• [11]Yaro A, Dao A, Adamou A, Crawford J, Ribeiro J, Gwadz R, Traore S, Lehmann T: The distribution of hatching time in Anopheles gambiae. Malar J 2006, 5:19. BioMed Central Full Text
• [12]Charlwood J, Vij R, Billingsley P: Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am J Trop Med Hyg 2000, 62(6):726.
• [13]Huestis DL, Traore AI, Dieter KL, Nwagbara JI, Bowie AC, Adamou A, Kassogue Y, Diallo M, Timbine S, Dao A: Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. Exp Bio 2012, 215(12):2013-2021.
• [14]Holstein MH: Biology of anopheles gambiae: research in French west Africa. Geneva: World Health Organization; 1954.
• [15]Omer S, Cloudsley-Thompson J: Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 1968, 217(2):879-880.
• [16]Kostal V, Sula J, Simek P: Physiology of drought tolerance and cold hardiness of the Mediterranean tiger moth Cymbalophora pudica during summer diapause. J Insect Physiol 1998, 44(2):165-173.
• [17]Benoit J, Morton P, Cambron S, Patrick K, Schemerhorn B: Aestivation and diapause syndromes reduce the water balance requirements for pupae of the Hessian fly, Mayetiola destructor. Entomol Exp Appl 2010, 136(1):89-96.
• [18]Tombes AS: Respiratory and compositional study on the aestivating insect, Hypera postica (Gyll.) (Curculionidae). J Insect Physiol 1964, 10(6):997-1003.
• [19]Jawara M, Pinder M, Drakeley C, Nwakanma D, Jallow E, Bogh C, Lindsay S, Conway D: Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar J 2008, 7(1):156. BioMed Central Full Text
• [20]Omer S, Cloudsley-Thompson J: Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull Wld Hlth Org 1970, 42(2):319-330.
• [21]Barnard D, Mulla M: Effects of photoperiod and temperature on blood feeding, oogenesis and fat body development in the mosquito, Culiseta inornata. J Insect Physiol 1977, 23(10):1261-1266.
• [22]Benoit J, Denlinger D: Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J Exp Bio 2007, 210(2):217.
• [23]Gibbs A, Chippindale A, Rose M: Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J Exp Bio 1997, 200(12):1821.
• [24]Nagpal B, Srivastava A, Kalra N, Subbarao S: Spiracular indices in Anopheles stephensi: a taxonomic tool to identify ecological variants. J Med Entomol 2003, 40(6):747-749.
• [25]Hadley NF: Water relations of terrestrial arthropods. San Diego, CA: Academic Press; 1994.
• [26]Stanley-Samuelson DW, Nelson DR: Insect lipids: chemistry, biochemistry, and biology. Lincoln, Nebraska: University of Nebraska Press; 1993.
• [27]Duncan F, Byrne M: The role of the mesothoracic spiracles in respiration in flighted and flightless dung beetles. J Exp Bio 2005, 208(5):907.
• [28]Blows MW, Hoffman AA: The genetics of central and marginal populations of Drosophila serrata. I. Genetic variation for stress resistance and species borders. Evolution 1993, 47(4):1255-1270.
• [29]Gibbs A, Fukuzato F, Matzkin L: Evolution of water conservation mechanisms in Drosophila. J Exp Bio 2003, 206(7):1183-1192.
• [30]Lehmann FO: Matching spiracle opening to metabolic need during flight in Drosophila. Science 2001, 294(5548):1926.
• [31]Lighton J: Discontinuous gas exchange in insects. Annu Rev Entomol 1996, 41(1):309-324.
• [32]Anderson J: Influence of photoperiod and temperature on the induction of diapause in Aedes atropalpus (Diptera: Culicidae). Entomol Exp Appl 1968, 11(3):321-330.
• [33]Holdgate M: Transpiration through the cuticles of some aquatic insects. J Exp Bio 1956, 33(1):107-118.
• [34]Koella JC, Lyimo EO: Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). J Med Entomol 1996, 33(2):261-264.
• [35]Huestis DL, Traoré AI, Adamou A, Kassogue Y, Diallo M, Timbine S, Dao A, Lehmann T: Variation in metabolic rate of Anopheles gambiae and A. arabiensis in a Sahelian village. J Exp Bio 2011, 214(14):2345-2353.
• [36]Jones B, Nachtsheim CJ: Split-plot designs: What, why, and how. J Qual Technol 2009, 41(4):340-361.
• [37]Caputo B, Dani F, Horne G, Petrarca V, Turillazzi S, Coluzzi M, Priestman A, Della Torre A: Identification and composition of cuticular hydrocarbons of the major Afrotropical malaria vector Anopheles gambiae ss (Diptera: Culicidae): analysis of sexual dimorphism and age-related changes. J Mass Spectrom 2005, 40(12):1595-1604.
• [38]Caputo B, Dani FR, Horne GL, N’Fale S, Diabate A, Turillazzi S, Coluzzi M, Costantini C, Priestman AA, Petrarca V, della Torre A: Comparative analysis of epicuticular lipid profiles of sympatric and allopatric field populations of Anopheles gambiae s.s. molecular forms and An. arabiensis from Burkina Faso (West Africa). Insect Biochem Molec 2007, 37(4):389-398.
• [39]Hugo LE, Kay BH, Eaglesham GK, Holling N, Ryan PA: Investigation of cuticular hydrocarbons for determining the age and survivorship of Australasian mosquitoes. Am J Trop Med Hyg 2006, 74(3):462-474.
• [40]Polerstock AR, Eigenbrode SD, Klowden MJ: Mating alters the cuticular hydrocarbons of female Anopheles gambiae sensu stricto and Aedes aegypti (Diptera: Culicidae). J Med Entomol 2002, 39(3):545-552.
• [41]Rockey S, Yoder J, Denlinger D: Reproductive and developmental consequences of a diapause maternal effect in the flesh fly, Sarcophaga bullata. Physiol Entomol 1991, 16(4):477-483.
• [42]Fouet C, Gray E, Besansky NJ, Costantini C: Adaptation to aridity in the malaria mosquito Anopheles gambiae: chromosomal inversion polymorphism and body size influence resistance to desiccation. PLoS One 2012, 7(4):e34841.
• [43]Lanciani C: Photoperiod and the relationship between wing length and body weight in Anopheles quadrimaculatus. J Am Mosquito Contr 1992, 8(3):297.
• [44]Alto B, Muturi E, Lampman R: Effects of nutrition and density in Culex pipiens. Med Vet Entomol 2012, 26(4):396-406.
• [45]Hood-Nowotny R, Schwarzinger B, Schwarzinger C, Soliban S, Madakacherry O, Aigner M, Watzka M, Gilles J: An analysis of diet quality, How it controls fatty acid profiles, isotope signatures and stoichiometry in the malaria mosquito Anopheles arabiensis. PLoS One 2012, 7(10):e45222.
• [46]Ohba SY, Ohtsuka M, Sunahara T, Sonoda Y, Kawashima E, Takagi M: Differential responses to predator cues between two mosquito species breeding in different habitats. Ecol Entomol 2012, 37(5):410-418.
• [47]Dodson BL, Kramer LD, Rasgon JL: Effects of larval rearing temperature on immature development and West Nile virus vector competence of Culex tarsalis. Parasit Vectors 2012, 5(1):1-6. BioMed Central Full Text
• [48]Araújo MS, Gil LHS: Larval food quantity affects development time, survival and adult biological traits that influence the vectorial capacity of Anopheles darlingi under laboratory conditions. Malar J 2012, 11(1):261. BioMed Central Full Text
• [49]Corkum LD, Hanes EC: Effects of temperature and photoperiod on larval size and survivorship of a burrowing mayfly (Ephemeroptera, Ephemeridae). Can J Zoolog 1992, 70(2):256-263.
• [50]Hanes EC, Ciborowski JJ: Effects of density and food limitation on size variation and mortality of larval Hexagenia rigida (Ephemeroptera: Ephemeridae). Can J Zoolog 1992, 70(9):1824-1832.
• [51]Agnew P, Hide M, Sidobre C, Michalakis Y: A minimalist approach to the effects of density-dependent competition on insect life-history traits. Ecol Entomol 2002, 27(4):396-402.
• [52]Muriu SM, Coulson T, Mbogo CM, Godfray HCJ: Larval density dependence in Anopheles gambiae ss, the major African vector of malaria. J Anim Ecol 2013, 82(1):166-174.
• [53]Gimnig JE, Ombok M, Otieno S, Kaufman MG, Vulule JM, Walker ED: Density-dependent development of Anopheles gambiae (Diptera: Culicidae) larvae in artificial habitats. J Med Entomol 2002, 39(1):162-172.
• [54]Cloudsley-Thompson JL: Adaptations of Arthropoda to arid environments. Annu Rev Entomol 1975, 20(1):261-283.
• [55]Urbanski JM, Benoit JB, Michaud MR, Denlinger DL, Armbruster P: The molecular physiology of increased egg desiccation resistance during diapause in the invasive mosquito, Aedes albopictus. P Roy Soc B-Biol Sci 2010, 277(1694):2683-2692.
• [56]Everaerts C, Farine J, Cobb M, Ferveur J: Drosophila cuticular hydrocarbons revisited: mating status alters cuticular profiles. PLoS One 2010, 5(3):e9607.
• [57]Verhoek B, Takken W: Age effects on the insemination rate of Anopheles gambiae sl in the laboratory. Entomol Exp Appl 1994, 72(2):167-172.
• [58]Joy TK, Gutierrez EHJ, Ernst K, Walker KR, Carriere Y, Torabi M, Riehle MA: Aging field collected Aedes aegypti to determine their capacity for dengue transmission in the Southwestern United States. PLoS One 2012, 7(10):e46946.
• [59]Dye C: The analysis of parasite transmission by bloodsucking insects. Annu Rev Entomol 1992, 37(1):1-19.
• [60]Brei B, Edman JD, Gerade B, Clark JM: Relative abundance of two cuticular hydrocarbons indicates whether a mosquito is old enough to transmit malaria parasites. J Med Entomol 2004, 41(4):807-809.