Ecophysiology of Anopheles gambiae s.l.: Persistence in the Sahel

Infection, Genetics and Evolution

Volumn 28, Issue , 2014, Pages 648-661

  Huestis, Diana L ^a   Lehmann, Tovi ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Aestivation; Diapause; Dormancy; Geographic variation; Malaria; Vector ecology

Indexed keywords

AEDES ALBOPICTUS; AESTIVATION; ANOPHELES GAMBIAE; ARTICLE; CARBOHYDRATE METABOLISM; DEVELOPING COUNTRY; DIAPAUSE; ECOPHYSIOLOGY; ENVIRONMENTAL CHANGE; ENVIRONMENTAL FACTOR; ENVIRONMENTAL IMPACT ASSESSMENT; GENE EXPRESSION; GEOGRAPHICAL VARIATION (SPECIES); HIGH TEMPERATURE; LIPID METABOLISM; METABOLIC RATE; NONHUMAN; PHOTOPERIODICITY; SEASONAL VARIATION; SUMMER; TROPIC CLIMATE; UPREGULATION; WINTER; ADAPTATION; AFRICA; ANIMAL; ASSOCIATION; ENERGY METABOLISM; ENVIRONMENT; INSECT VECTOR; MALARIA; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REPRODUCTION; SEASON; TRANSMISSION;

ANOPHELES GAMBIAE;

ADAPTATION, BIOLOGICAL; AFRICA, NORTHERN; ANIMALS; ANOPHELES GAMBIAE; CUES; DIAPAUSE, INSECT; ENERGY METABOLISM; ENVIRONMENT; INSECT VECTORS; MALARIA; REPRODUCTION; SEASONS; STRESS, PHYSIOLOGICAL;

EID: 84912064659     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2014.05.027     Document Type: Article

References (145)

1. Aboagye-Antwi F., Tripet F. Effects of larval growth condition and water availability on desiccation resistance and its physiological basis in adult Anopheles gambiae sensu stricto. Malar. J. 2010, 9:225.
2. Adamou A., Dao A., Timbine S., Kassogue Y., Yaro A.S., Diallo M., Traore S.F., Huestis D.L., Lehmann T. The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel. Malar. J. 2011, 10:151.
3. Andrewartha H.G. Diapause in relation to the ecology of insects. Biol. Rev. Camb. Philos. Soc. 1952, 27:50-107.
4. Artis M.L., Huestis D.L., Lehmann T. The effects of oviposition-site deprivation on longevity and bloodfeeding rate in Anopheles gambiae. Parasit. Vectors 2014, 7:163.
5. Barnard D.R., Mulla M.S. Effects of photoperiod and temperature on blood feeding, oogenesis, and fat body development in the mosquito, Culiseta inornata. J. Insect Physiol. 1977, 23:1261-1266.
6. Barnard D.R., Mulla M.S. The ecology of Culiseta inornata in the Colorado Desert of California: seasonal abundance, gonotrophic status, and oviparity of adult mosquitoes. Ann. Entomol. Soc. Am. 1978, 71:397-401.
7. Bates M. The Natural History of Mosquitoes 1949, MacMillan, New York.
8. Bayoh M.N., Thomas C.J., Lindsay S.W. Mapping distributions of chromosomal forms of Anopheles gambiae in West Africa using climate data. Med. Vet. Entomol. 2001, 15:267-274.
9. Beach R. Required day number and timely induction of diapause in geographic strains of mosquito Aedes atropalpus. J. Insect Physiol. 1978, 24:449-455.
10. Beier J.C., Copeland R.S., Oyaro C., Masinya A., Odago W.O., Odour S., Koech D.K., Roberts C.R. Anopheles gambiae complex egg stage survival in dry soil from larval development sites in western Kenya. J. Am. Mosq. Control Assoc. 1990, 6:105-109.
11. Benedict M.Q., Sandve S.R., Wilkins E.E., Roberts J.M. Relationship of larval desiccation to Anopheles gambiae Giles and An. arabiensis Patton survival. J. Vector. Ecol. 2010, 35:116-123.
12. Bennett V.A., Kukal O., Lee R.E. Metabolic opportunists: feeding and temperature influence the rate and pattern of respiration in the high arctic woollybear caterpillar Gynaephora groenlandica (Lymantriidae). J. Exp. Biol. 1999, 202:47-53.
13. Benoit J.B., Denlinger D.L. Suppression of water loss during adult diapause in the northern house mosquito, Culex pipiens. J. Exp. Biol. 2007, 210:217-226.
14. Benoit J.B., Lopez-Martinez G., Phillips Z.P., Patrick K.R., Denlinger D.L. Heat shock proteins contribute to mosquito dehydration tolerance. J. Insect Physiol. 2010, 56:151-156.
15. Benoit J.B., Patrick K.R., Desai K., Hardesty J.J., Krause T.B., Denlinger D.L. Repeated bouts of dehydration deplete nutrient reserves and reduce egg production in the mosquito Culex pipiens. J. Exp. Biol. 2010, 213:2763-2769.
16. Bradshaw W.E., Lounibos L.P. Evolution of dormancy and its photoperiodic control in pitcher-plant mosquitoes. Evolution 1977, 31:546-567.
17. Brakefield P.M., Pijpe J., Zwaan B.J. Developmental plasticity and acclimation both contribute to adaptive responses to alternating seasons of plenty and of stress in Bicyclus butterflies. J. Biosci. 2007, 32:465-475.
18. Brent C.S., Klok C.J., Naranjo S.E. Effect of diapause status and gender on activity, metabolism, and starvation resistance in the plant bug Lygus hesperus. Entomol. Exp. Appl. 2013, 148:152-160.
19. Buth J.L., Brust R.A., Ellis R.A. Development time, oviposition activity and onset of diapause in Culex tarsalis, Culex restuans, and Culiseta inornata in southern Manitoba. J. Am. Mosq. Control Assoc. 1990, 6:55-63.
20. Canzano A.A., Krockenberger A.A., Jones R.E., Seymour J.E. Rates of metabolism in diapausing and reproductively active tropical butterflies, Euploea core and Euploea sylvester (Lepidoptera: Nymphalidae). Physiol. Entomol. 2006, 31:184-189.
21. Chambers R.J. Maternal experience of crowding and duration of aestivation in the sycamore aphid. Oikos 1982, 39:100-102.
22. Charlwood J.D., Vij R., Billingsley P.F. Dry season refugia of malaria-transmitting mosquitoes in a dry savannah zone of east Africa. Am. J. Trop. Med. Hyg. 2000, 62:726-732.
23. Charlwood J.D., Cuamba N., Tomas E.V., Briet O.J. Living on the edge: a longitudinal study of Anopheles funestus in an isolated area of Mozambique. Malar. J. 2013, 12:208.
24. Chown S.L. Respiratory water loss in insects. Comparative biochemistry and physiology A-molecular and integrative physiology 2002, 133:791-804.
25. Chown S.L., Nicolson S.W. Insect Physiological Ecology: Mechanisms and Patterns 2004, Oxford University Press, Oxford.
26. Clarke A., Fraser K.P.P. Why does metabolism scale with temperature?. Funct. Ecol. 2004, 18:243-251.
27. Clements A.N. The Physiology of Mosquitoes 1963, Pergamon Press, Oxford.
28. Clements A.N. The Biology of Mosquitoes 1992, Chapman & Hall, London.
29. Coetzee M., Hunt R.H., Wilkerson R., Della Torre A., Coulibaly M.B., Besansky N.J. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa 2013, 3619:246-274.
30. Coluzzi M. Morphological divergences in the Anopheles gambiae complex. Riv. Malariol. 1964, 43:197-232.
31. Coluzzi M., Sabatini A., Petrarca V., Di Deco M.A. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans. R. Soc. Trop. Med. Hyg. 1979, 73:483-497.
32. Coluzzi M., Petrarca V., Di Deco M.A. Chromosomal inversion intergradation and incipient speciation in Anopheles gambiae. Boll. Zool. 1985, 52:45-63.
33. Daibo S., Kimura M.T., Goto S.G. Upregulation of genes belonging to the drosomycin family in diapausing adults of Drosophila triauraria. Gene 2001, 278:177-184.
34. Danilevskii A.S. Photoperiodism and Seasonal Development of Insects 1965, Oliver and Boyd, Edinburgh and London.
35. Davidson G. Anopheles gambiae, a complex of species. Bull. World Health Organ. 1964, 31:625-634.
36. Denlinger D.L. Dormancy in tropical insects. Annu. Rev. Entomol. 1986, 31:239-264.
37. Denlinger D.L. Regulation of diapause. Annu. Rev. Entomol. 2002, 47:93-122.
38. Denlinger D.L., Armbruster P.A. Mosquito diapause. Annu. Rev. Entomol. 2014, 59:73-93.
39. Depner K.R., Harwood R.F. Photoperiodic responses of 2 latitudinally diverse groups of Anopheles freeborni (Diptera - Culicidae). Ann. Entomol. Soc. Am. 1966, 59:7-11.
40. Dieter K.L., Huestis D.L., Lehmann T. The effects of oviposition-site deprivation on Anopheles gambiae reproduction. Parasit. Vectors 2012, 5:235.
41. Dingle H. Migration: The Biology of Life on the Move 1996, Oxford University Press, New York.
42. Dixon A.F.G. The effect of population density and nutritive status of the host on the summer reproductive activity of the sycamore aphid, Drepanosiphum platanoides (Schr.). J. Anim. Ecol. 1966, 35:105-112.
43. Dixon A.F.G., Wellings P.W., Carter C., Nichols J.F.A. The role of food quality and competition in shaping the seasonal cycle in the reproductive activity of the sycamore aphid. Oecologia 1993, 95:89-92.
44. Djawdan M., Rose M.R., Bradley T.J. Does selection for stress resistance lower metabolic rate?. Ecology 1997, 78:828-837.
45. Donnelly M.J., Simard F., Lehmann T. Evolutionary studies of malaria vectors. Trends Parasitol. 2002, 18:75-80.
46. Douglas A.E. Reproductive diapause and the bacterial symbiosis in the sycamore aphid Drepanosiphum platanoidis (Schr.). Ecol. Entomol. 2000, 25:256-261.
47. Eldridge B.F. Diapause and Related Phenomena in Culex Mosquitoes: Their Relation to Arbovirus Disease Ecology, Current Topics in Vector Research 1987, 1-28. Springer, New York.
48. Emerson K.J., Bradshaw W.E., Holzapfel C.M. Complications of complexity: integrating environmental, genetic and hormonal control of insect diapause. Trends Genet. 2009, 25:217-225.
49. Focks D.A., Linda S.B., Craig G.B., Hawley W.H., Pumpuni C.B. Aedes albopictus (Diptera: Culicidae): a statistical model of the role of temperature, photoperiod, and geography in the induction of egg diapause. J. Med. Entomol. 1994, 31:276-286.
50. Fouet C., Gray E., Besansky N.J., 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:e34841.
51. Gibbs A.G., Johnson R.A. The role of discontinuous gas exchange in insects: the chthonic hypothesis does not hold water. J. Exp. Biol. 2004, 207:3477-3482.
52. Gibbs A.G., Chippindale A.K., Rose M.R. Physiological mechanisms of evolved desiccation resistance in Drosophila melanogaster. J. Exp. Biol. 1997, 200:1821-1832.
53. Gibbs A.G., Fukuzato F., Matzkin L.M. Evolution of water conservation mechanisms in Drosophila. J. Exp. Biol. 2003, 206:1183-1192.
54. Gillies M.T., De Meillon B. The Anophelinae of Africa south of the Sahara 1968, South African Institute for Medical Research, Johannesburg, South Africa. second ed.
55. Gray E.M., Bradley T.J. Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis. Am. J. Trop. Med. Hyg. 2005, 73:553-559.
56. Gray E.M., Rocca K.A., Costantini C., Besansky N.J. Inversion 2La is associated with enhanced desiccation resistance in Anopheles gambiae. Malar. J. 2009, 8:215.
57. Guppy M. The biochemistry of metabolic depression: a history of perceptions. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2004, 139:435-442.
58. Guppy M., Withers P. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. Camb. Philos. Soc. 1999, 74:1-40.
59. Hadley N.F. Ventilatory patterns and respiratory transpiration in adult terrestrial insects. Physiol. Zool. 1994, 67:175-189.
60. Hahn D.A., Denlinger D.L. Energetics of insect diapause. Annual Review of Entomology 2011, vol. 56:103-121. Annual Reviews, Palo Alto.
61. Hairston N.G., Kearns C.M. The interaction of photoperiod and temperature in diapause timing - a copepod example. Biol. Bull. 1995, 189:42-48.
62. Hao Y.J., Li W.S., He Z.B., Si F.L., Ishikawa Y., Chen B. Differential gene expression between summer and winter diapause pupae of the onion maggot Delia antiqua, detected by suppressive subtractive hybridization. J. Insect Physiol. 2012, 58:1444-1449.
63. Harwood R.F., Halfhill E. The effect of photoperiod on fat body and ovarian development of Culex tarsalis (Diptera: Culicidae). Ann. Entomol. Soc. Am. 1964, 57:596-600.
64. Held C., Spieth H.R. First evidence of pupal summer diapause in Pieris brassicae L.: the evolution of local adaptedness. J. Insect Physiol. 1999, 45:587-598.
65. Holstein M.H. Biology of Anopheles gambiae 1954, Research in French West Africa, World Health Organization, Geneva.
66. Hudson J.E. Induction of diapause in female mosquitoes, Culiseta inornata, by a decrease in daylength. J. Insect Physiol. 1977, 23:1377-1382.
67. Huestis D.L., Yaro A.S., Traore A.I., 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. Biol. 2011, 214:2345-2353.
68. Huestis D.L., Yaro A.S., Traore A.I., Dieter K.L., Nwagbara J.I., Bowie A.C., Adamou A., Kassogue Y., Diallo M., Timbine S., Dao A., Lehmann T. Seasonal variation in metabolic rate, flight activity and body size of Anopheles gambiae in the Sahel. J. Exp. Biol. 2012, 215:2013-2021.
69. Ikeno T., Tanaka S.I., Numata H., Goto S.G. Photoperiodic diapause under the control of circadian clock genes in an insect. BMC Biol. 2010, 8.
70. Jaenson T.G.T., Ameneshewa B. Prehibernation diet and reproductive condition of female Anopheles messeae in Sweden. Med. Vet. Entomol. 1991, 5:243-252.
71. Jawara M., Pinder M., Drakeley C.J., Nwakanma D.C., Jallow E., Bogh C., Lindsay S.W., Conway D.J. Dry season ecology of Anopheles gambiae complex mosquitoes in The Gambia. Malar. J. 2008, 7:156.
72. Jetten, T.H., Takken, W., 1994. Anophelism without malaria in Europe: a review of the ecology and distribution of the genus Anopheles in Europe. Wageningen Agricultural University Papers 94-5, pp. 1-69.
73. Kaufmann C., Briegel H. Flight performance of the malaria vectors Anopheles gambiae and Anopheles atroparvus. J. Vector Ecol. 2004, 29:140-153.
74. Keilin D. The problem of anabiosis or latent life: history and current concept. Proc. R. Soc. Lond. B Biol. Sci. 1959, 150:149-191.
75. Kim M., Denlinger D.L. Decrease in expression of beta-tubulin and microtubule abundance in flight muscles during diapause in adults of Culex pipiens. Insect Mol. Biol. 2009, 18:295-302.
76. Kim M., Robich R.M., Rinehart J.P., Denlinger D.L. Upregulation of two actin genes and redistribution of actin during diapause and cold stress in the northern house mosquito, Culex pipiens. J. Insect Physiol. 2006, 52:1226-1233.
77. Kirby M.J., Lindsay S.W. Responses of adult mosquitoes of two sibling species, Anopheles arabiensis and A. gambiae s.s. (Diptera: Culicidae), to high temperatures. Bull. Entomol. Res. 2004, 94:441-448.
78. Koenraadt C.J., Paaijmans K.P., Githeko A.K., Knols B.G., Takken W. Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats. Malar. J. 2003, 2:20.
79. Kostal V. Eco-physiological phases of insect diapause. J. Insect Physiol. 2006, 52:113-127.
80. Kostal V., Hodek I. Photoperiodism and control of summer diapause in the Mediterranean tiger moth Cymbalophora pudica. J. Insect Physiol. 1997, 43:767-777.
81. Kostal V., Simek P. Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 1998, 168:453-460.
82. 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, 44:165-173.
83. Lanciani C.A. Photoperiod and longevity in Anopheles crucians. J. Am. Mosq. Control Assoc. 1993, 9:308-312.
84. Lanciani C.A., Anderson J.F. Effect of photoperiod on longevity and metabolic rate in Anopheles quadrimaculatus. J. Am. Mosq. Control Assoc. 1993, 9:158-163.
85. Lee Y., Meneses C.R., Fofana A., Lanzaro G.C. Desiccation resistance among subpopulations of Anopheles gambiae s.s. From Selinkenyi, Mali. J. Med. Entomol. 2009, 46:316-320.
86. Lehmann T., Diabate A. The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect. Genet. Evol. 2008, 8:737-746.
87. Lehmann T., Dao A., Yaro A.S., Adamou A., Kassogue Y., Diallo M., Sekou T., Coscaron-Arias C. Aestivation of the African malaria mosquito, Anopheles gambiae, in the Sahel. Am. J. Trop. Med. Hyg. 2010, 83:601-606.
88. Lehmann T., Dao A., Yaro A.S., Diallo M., Timbine S., Huestis D.L., Adamou A., Kassogue Y., Traore A.I. Seasonal variation in spatial distributions of Anopheles gambiae in a Sahelian village: evidence for aestivation. J. Med. Entomol. 2014, 51:27-38.
89. Lemasson J.J., Fontenille D., Lochouarn L., Dia I., Simard F., Ba K., Diop A., Diatta M., Molez J.F. Comparison of behavior and vector efficiency of Anopheles gambiae and An. arabiensis (Diptera: Culicidae) in Barkedji, a Sahelian area of Senegal. J. Med. Entomol. 1997, 34:396-403.
90. Lighton J.R.B. Discontinuous gas exchange in insects. Annu. Rev. Entomol. 1996, 41:309-324.
91. Liu Z.D., Gong P.Y., Wu K.J., Sun J.H., Li D.M. A true summer diapause induced by high temperatures in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae). J. Insect Physiol. 2006, 52:1012-1020.
92. Lounibos L.P., Escher R.L., Lourenco-de-Oliveria R. Asymmetric evolution of photoperiodic diapause in temperate and tropical invasive populations of Aedes albopictus (Diptera: Culicidae). Ann. Entomol. Soc. Am. 2003, 96:512-518.
93. Lounibos L.P., Escher R.L., Nishimura N. Retention and adaptiveness of photoperiodic egg diapause in Florida populations of invasive Aedes albopictus. J. Am. Mosq. Control Assoc. 2011, 27:433-436.
94. Luker L.A., Hatle J.D., Juliano S.A. Reproductive responses to photoperiod by a south Florida population of the grasshopper Romalea microptera (Orthoptera: Romaleidae). Environ. Entomol. 2002, 31:702-707.
95. MacRae T.H. Gene expression, metabolic regulation and stress tolerance during diapause. Cell. Mol. Life Sci. 2010, 67:2405-2424.
96. Mamai W., Mouline K., Blais C., Larvor V., Dabire K.R., Ouedraogo G.A., Simard F., Renault D. Metabolomic and ecdysteroid variations in Anopheles gambiae s.l. mosquitoes exposed to the stressful conditions of the dry season in Burkina Faso, West Africa. Physiol. Biochem. Zool. 2014, 87:486-497.
97. Masaki S. Summer diapause. Annu. Rev. Entomol. 1980, 25:1-25.
98. Minakawa N., Githure J.I., Beier J.C., Yan G.Y. Anopheline mosquito survival strategies during the dry period in western Kenya. J. Med. Entomol. 2001, 38:388-392.
99. Nagpal B.N., Srivastava A., Kalra N.L., Subbarao S.K. Spiracular indices in Anopheles stephensi: a taxonomic tool to identify ecological variants. J. Med. Entomol. 2003, 40:747-749.
100. Omer S.M., Cloudsley-Thompson J.L. Dry season biology of Anopheles gambiae Giles in the Sudan. Nature 1968, 217:879-880.
101. Omer S.M., Cloudsley-Thompson J.L. Survival of female Anopheles gambiae Giles through a 9-month dry season in Sudan. Bull. World Health Organ. 1970, 42:319-330.
102. Poelchau M.F., Reynolds J.A., Elsik C.G., Denlinger D.L., Armbruster P.A. Deep sequencing reveals complex mechanisms of diapause preparation in the invasive mosquito, Aedes albopictus. Proc. R. Soc. B Biol. Sci. 2013, 280.
103. Poelchau M.F., Reynolds J.A., Elsik C.G., Denlinger D.L., Armbruster P.A. RNA-Seq reveals early distinctions and late convergence of gene expression between diapause and quiescence in the Asian tiger mosquito, Aedes albopictus. J. Exp. Biol. 2013, 216:4082-4090.
104. Pullin A.S., Wolda H. Glycerol and glucose accumulation during diapause in a tropical beetle. Physiol. Entomol. 1993, 18:75-78.
105. Ragland G.J., Fuller J., Feder J.L., Hahn D.A. Biphasic metabolic rate trajectory of pupal diapause termination and post-diapause development in a tephritid fly. J. Insect Physiol. 2009, 55:344-350.
106. Ramsdale, C.D., Fontaine, R.E., 1970a. Ecological investigations of Anopheles gambiae and Anopheles funestus II. Dry season studies with colony-reared A. gambiae species B, Kaduna Nigeria. WHO/VBC/70.249, pp. 1-8.
107. Ramsdale, C.D., Fontaine, R.E., 1970b. Ecological investigations of Anopheles gambiae and Anopheles funestus I. Dry season studies in villages near Kaduna Nigeria. WHO/VBC/70.248.
108. Rao V.V. On gonotrophic discordance among certain Indian Anopheles. Indian J. Malariol. 1947, 1:43-50.
109. Reisen W.K., Meyer R.P., Milby M.M. Studies on the seasonality of Culiseta inornata in Kern County, California. J. Am. Mosq. Control Assoc. 1989, 5:183-195.
110. Reisen W.K., Thiemann T., Barker C.M., Lu H.L., Carroll B., Fang Y., Lothrop H.D. Effects of warm winter temperature on the abundance and gonotrophic activity of Culex (Diptera: Culicidae) in California. J. Med. Entomol. 2010, 47:230-237.
111. Robich R.M., Denlinger D.L. Diapause in the mosquito Culex pipiens evokes a metabolic switch from blood feeding to sugar gluttony. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15912-15917.
112. Rocca K.A.C., Gray E.M., Costantini C., Besansky N.J. 2La chromosomal inversion enhances thermal tolerance of Anopheles gambiae larvae. Malar. J. 2009, 8:147.
113. Sim C., Denlinger D.L. Insulin signaling and FOXO regulate the overwintering diapause of the mosquito Culex pipiens. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:6777-6781.
114. Sim C., Denlinger D.L. A shut-down in expression of an insulin-like peptide, ILP-1, halts ovarian maturation during the overwintering diapause of the mosquito Culex pipiens. Insect Mol. Biol. 2009, 18:325-332.
115. Simard F., Lehmann T., Lemasson J.J., Diatta M., Fontenille D. Persistence of Anopheles arabiensis during the severe dry season conditions in Senegal: an indirect approach using microsatellite loci. Insect Mol. Biol. 2000, 9:467-479.
116. Sinclair B.J., Bretman A., Tregenza T., Tomkins J.L., Hosken D.J. Metabolic rate does not decrease with starvation in Gryllus bimaculatus when changing fuel use is taken into account. Physiol. Entomol. 2011, 36:84-89.
117. Sogoba N., Doumbia S., Vounatsou P., Baber I., Keita M., Maiga M., Traore S.F., Toure A., Dolo G., Smith T., Ribeiro J.M.C. Monitoring of larval habitats and mosquito densities in the Sudan savanna of Mali: implications for malaria vector control. Am. J. Trop. Med. Hyg. 2007, 77:82-88.
118. Spielman A. Effect of synthetic juvenile hormone on ovarian diapause of Culex pipiens mosquitoes. J. Med. Entomol. 1974, 11:223-225.
119. Spielman A. Structure and seasonality of nearctic Culex pipiens populations. West Nile Virus: Detection, Surveillance, and Control 2001, 220-234. New York Acad Sciences, New York. D.J. White, D.L. Morse (Eds.).
120. Spielman A., Wong J. Environmental control of ovarian diapause in Culex pipiens (Diptera: Culicidae). Ann. Entomol. Soc. Am. 1973, 66:905-907.
121. Storey K.B., Storey J.M. Metabolic rate depression and biochemical adaptation in anaerobiosis, hibernation, and estivation. Q. Rev. Biol. 1990, 65:145-174.
122. Storey K.B., Storey J.M. Metabolic rate depression in animals: transcriptional and translational controls. Biol. Rev. 2004, 79:207-233.
123. Storey K.B., Storey J.M. Aestivation: signaling and hypometabolism. J. Exp. Biol. 2012, 215:1425-1433.
124. Sun J., Mu H.W., Zhang H.M., Chandramouli K.H., Qian P.Y., Wong C.K.C., Qiu J.W. Understanding the regulation of estivation in a freshwater snail through iTRAQ-based comparative proteomics. J. Proteome Res. 2013, 12:5271-5280.
125. Swellengrebel N.H. La dissociation des fonctions sexuelles de nutritives (dissociation gonotrophique) d'Anopheles maculipennis comme cause du paludisme dans les Pays-Bas et ses rapports ave 'l'infection domiciliare'. Ann. Inst. Pasteur 1929, 43:1370-1389.
126. Tauber M.J., Tauber C.A., Masaki S. Seasonal Adaptations of Insects 1986, Oxford University Press, New York.
127. Tauber M.J., Tauber C.A., Nyrop J.P., Villani M.G. Moisture, a vital but neglected factor in the seasonal ecology of insects: hypotheses and tests of mechanisms. Environ. Entomol. 1998, 27:523-530.
128. Tombes A.S. Respiratory and compositional study on the aestivating insect, Hypera postica (Gyll) (Curculionidae). J. Insect Physiol. 1964, 10:997-1003.
129. Toure Y.T., Petrarca V., Traore S.F., Coulibaly A., Maiga H.M., Sankare O., Sow M., Di Deco M.A., Coluzzi M. Ecological genetic studies in the chromosomal form Mopti of Anopheles gambiae s.str. in Mali, West Africa. Genetica 1994, 94:213-223.
130. Tsuda Y., Kim K.S. Sudden autumnal appearance of adult Culex tritaeniorhynchus (Diptera: Culicidae) at a park in urban Tokyo: first field evidence for prediapause migration. J. Med. Entomol. 2008, 45:610-616.
131. Urbanski J., Mogi M., O'Donnell D., DeCotiis M., Toma T., Armbruster P. Rapid adaptive evolution of photoperiodic response during invasion and range expansion across a climatic gradient. Am. Nat. 2012, 179:490-500.
132. Vinogradova An experimental investigation of the ecological factors inducing imaginal diapause in blood sucking mosquitoes. Entomol. Rev. 1960, 39:210-219.
133. Vinogradova E.B., Pantyuchov G.A. Adult diapause and its physiological characteristic in the ragweed leaf beetle, Zygogramma suturalis F (Coleoptera, Chrysomelidae), introduced to Russia from north America. Folia Biol. (Krakow) 1995, 43:137-141.
134. Vinogradova E.B., De Statsio B., Gilbert J.J. Diapause in aquatic insects, with emphasis on mosquitoes. Diapause in Aquatic Invertebrates 2007, 83-113. Springer. V.R. Alekseev (Ed.).
135. Wachira S.W., Ndung'u M., Njagi P.G.N., Hassanali A. Comparative responses of ovipositing Anopheles gambiae and Culex quinquefasciatus females to the presence of Culex egg rafts and larvae. Med. Vet. Entomol. 2010, 24:369-374.
136. Wagoner K.M., Lehmann T., Huestis D.L., Cech N.B., Ehrmann B.M., Wasserberg G. Identification of morphologic and chemical markers of dry- and wet-season conditions in female Anopheles gambiae mosquitoes. Parasit. Vectors 2014, 7:294. 10.1186/1756-3305-7-294.
137. Wang M.H., Marinotti O., James A.A., Walker E., Githure J., Yan G.Y. Genome-wide patterns of gene expression during aging in the African malaria vector Anopheles gambiae. PLoS ONE 2010, 5:e13359.
138. Wang M.H., Marinotti O., Vardo-Zalik A., Boparai R., Yan G.Y. Genome-wide transcriptional analysis of genes associated with acute desiccation stress in Anopheles gambiae. PLoS ONE 2011, 6:e26011.
139. Washino R.K. Physiological condition of overwintering female Anopheles freeborni in California (Diptera: Culicidae). Ann. Entomol. Soc. Am. 1970, 63:210.
140. Washino R.K. The physiological ecology of gonotrophic dissociation and related phenomena in mosquitoes. J. Med. Entomol. 1977, 13:381-388.
141. Washino R.K., Bailey S.F. Overwintering of Anopheles punctipennis (Diptera: Culicidae) in California. J. Med. Entomol. 1970, 7:95.
142. WHO World Malaria Report 2013 2013, World Health Organization, Geneva, Switzerland.
143. Yaro A.S., Traore A.I., Huestis D.L., Adamou A., Timbine S., Kassogue Y., Diallo M., Dao A., Traore S.F., Lehmann T. Dry season reproductive depression of Anopheles gambiae in the Sahel. J. Insect Physiol. 2012, 58:1050-1059.
144. Zhou G.L., Miesfeld R.L. Energy metabolism during diapause in Culex pipiens mosquitoes. J. Insect Physiol. 2009, 55:40-46.
145. Zhu H.S., Casselman A., Reppert S.M. Chasing migration genes: a brain expressed sequence tag resource for summer and migratory monarch butterflies (Danaus plexippus). PLoS ONE 2008, 3:e1345.