The molecular physiology of increased egg desiccation resistance during diapause in the invasive mosquito, Aedes albopictus

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1694, 2010, Pages 2683-2692

  Urbanski, Jennifer M ^a   Benoit, Joshua B ^b   Michaud, M Robert ^b   Denlinger, David L ^b   Armbruster, Peter ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Aedes albopictus; Desiccation resistance; Invasive species; Photoperiodic diapause

Indexed keywords

ABUNDANCE; ADAPTATION; DESICCATION; EVOLUTIONARY BIOLOGY; FATTY ACID; INVASIVE SPECIES; MOSQUITO; PHOTOPERIOD; SEASONAL VARIATION;

AEDES ALBOPICTUS; ARTHROPODA;

EID: 77956897665     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.0362     Document Type: Conference Paper

References (60)

1. Armbruster, P. & Conn, J. E. 2006 Geographic variation of larval growth in North American Aedes albopictus (Diptera: Culicidae). Ann. Entomol. Soc. Am. 99, 1234-1243. (doi:10.1603/0013-8746(2006)99[1234:GVOLGI]2.0. CO;2)
2. Armold, M. T. & Regnier, F. E. 1975 Developmental study of cuticular hydrocarbons of Sarcophaga bullata. J. Insect Physiol. 21, 1827-1833. (doi:10.1016/0022-1910(75)90249-8)
3. Beckel, W. E. 1958 Investigations of impermeability, diapause, and hatching in the eggs of the mosquito Aedes hexodontus. Can. J. Zool. 36, 541-554. (doi:10.1139/ z58-050)
4. Bell, R. A., Nelson, P. R., Borg, T. K. & Caldwell, D. L. 1975 Wax secretion in non-diapausing and diapausing pupae of the tobacco hornworm Manduca sexta. J. Insect Physiol. 21, 1725-1799. (doi:10.1016/0022-1910(75) 90186-9)
5. Benedict, M. Q., Levine, R. S., Hawley, W. A. & Lounibos, L. P. 2007 Spread of the tiger: Global risk of invasion by the mosquito Aedes albopictus. Vector-borne Zoonotic Dis. 7, 76-85. (doi:10.1089/vbz.2006.0562) (Pubitemid 46626693)
6. Benoit, J. B. & Denlinger, D. L. 2007 Suppression of water loss during adult diapause in the northern house mosquito Culex pipiens. J. Exp. Biol. 210, 217-226. (doi:10. 1242/jeb.02630)
7. Benoit, J. B., Lopez-Martinez, G., Elnitsky, M. A., Lee Jr, R. E. & Denlinger, D. L. 2009 Dehydration-induced cross tolerance of Belgica antarctica larvae to cold and heat is facilitated by trehalose accumulation. Comp. Bio-chem. Physiol. A 152, 518-523. (doi:10.1016/j.cbpa. 2008.12.009)
8. Blomquist, G. J., Nelson, D. R. & de Renobales, M. 1987 Chemistry, biochemistry and physiology of insect cuticu-lar lipids. Arch. Insect. Biochem. Physiol. 6, 227-265. (doi:10.1002/arch.940060404)
9. Clements, A. N. 1992 The biology of mosquitoes: development, nutrition and reproduction. London, UK: Chapman and Hall.
10. Coudron, T. A. & Nelson, D. R. 1981 Characterization and distribution of the hydrocarbons found in diapausing pupae tissues of the tobacco hornworm, Manduca sexta L. J. Lipid Res. 22, 103-112.
11. Denlinger, D. L. 2002 Regulation of diapause. Annu. Rev. Entomol. 47, 93-122. (doi:10.1146/annurev.ento.47. 091201.145137) (Pubitemid 34108577)
12. Faith, D. P., Minchin, P. R. & Belbin, L. 1987 Compositional dissimilarity as a robust measure of ecological distance. Vegetation 69, 57-68. (doi:10.1007/ BF00038687)
13. Foley, B., Chenoweth, S. F., Nuzhdin, S. V. & Blows, M. W. 2007 Natural genetic variation in cuticular hydrocarbon expression in male and female Drosophila melanogaster. Genetics 175, 1465-1477. (doi:10.1534/genetics.106. 065771) (Pubitemid 46798245)
14. Gibbs, A. G. 1998 Water-proofing properties of cuticular lipids. Am. Zool. 38, 471-482. (doi:10.1093/icb/38.3. 471)
15. Goltsev, Y., Rezende, G. L., Vranizan, K., Lanzaro, G., Valle, D. & Levine, M. 2009 Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo. Dev. Biol. 330, 462-470. (doi:10.1016/ j.ydbio.2009.02.038)
16. Goto, S. G., Han, B. & Denlinger, D. L. 2006 A nondiapaus-ing variant of the flesh fly, Sarcophaga bullata, that shows arrhythmic adult eclosion and elevated expression of two circadian clock genes, period and timeless. J. Insect Phy-siol. 52, 1213-1218. (doi:10.1016/j.jinsphys.2006.09. 003) (Pubitemid 44750000)
17. Gratz, N. G. 2004 Critical review of the vector status of Aedes albopictus. Med. Vet. Entomol. 18, 215-227. (doi:10.1111/ j.0269-283X.2004. 00513.x)
18. Gray, E. M. & Bradley, T. J. 2005 Physiology of desiccation resistance in Anopheles gambiae and Anopheles arabiensis. Am. J. Trop. Med. Hyg. 73, 553-559.
19. Hadley, N. F. 1994 Water relations of terrestrial arthropods. San Diego, CA: Academic Press.
20. Hanson, S. M. & Craig, G. B. 1994 Cold acclimation, diapause, and geographic origin affect cold hardiness in eggs of Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 31, 192-201.
21. Hawley, W. A. 1988 The biology of Aedes albopictus. J. Am. Mosq. Control Assoc. 4, 1-39.
22. Hawley, W. A., Reiter, P., Copeland, R. S., Pumpuni, C. B. & Craig, G. B. 1987 Aedes albopictus in North America-probable introduction in used tires from northern Asia. Science 236, 1114-1116. (doi:10.1126/science. 3576225)
23. Joyce, C. R. 1961 Potentialities for accidental establishment of exotic mosquitoes in Hawaii. Proc. Hawaii Entomol. Soc. 17, 407-413.
24. Juárez, P. 1994 Hydrocarbon biosynthesis in Triatoma infes-tans. Arch. Insect Biochem. Physiol. 25, 193-206. (doi:10. 1002/arch.940250303)
25. Juárez, M. P. 2004 Fatty acyl-CoA elongation in Blatella ger-manica integumental microsomes. Arch. Insect Biochem. Physiol. 56, 170-178. (doi:10.1002/arch.20007) (Pubitemid 39123206)
26. Juárez, M. P. & Fernández, G. C. 2007 Cuticular hydrocarbons of triatomines. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 147, 711-730. (doi:10.1016/j.cbpa.2006. 08.031) (Pubitemid 46755605)
27. Juliano, S. A. & Lounibos, L. P. 2005 Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol. Lett. 8, 558-574. (doi:10.1111/j.1461-0248.2005.00755.x) (Pubitemid 40641145)
28. Juliano, S. A., O'Meara, G. F., Morrill, J. R. & Cutwa, M. M. 2002 Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia 130, 458-469. (doi:10.1007/s004420100811) (Pubitemid 36059225)
29. Jurenka, R. A., Holland, D. & Krafsur, E. S. 1998 Hydrocarbon profiles of diapausing and reproductive adult face flies (Musca autumnalis). Arch. Insect Biochem. Physiol. 37, 206-214. (doi:10.1002/(SICI)1520-6327 (1998)37:3,206:AID-ARCH3.3.0.CO;2-Q)
30. Kaneko, J. & Katagiri, C. 2004 Epicuticular wax of large and small white butterflies, Pieris brassicae and Prapae cruci-vora: qualitative and quantitative comparison between diapause and non-diapause pupae. Naturwissenschaften 91, 320-323. (doi:10.1007/s00114-004-0535-7)
31. Livak, K. J. & Schmittgen, T. D. 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. (doi:10.1006/meth.2001.1262) (Pubitemid 34164012)
32. Major, M. A. & Blomquist, G. J. 1978 Biosynthesis of hydrocarbons in insects. Decarboxylation of long chain acid to n-alkanes in Periplaneta. Lipids 13, 323-328. (doi:10. 1007/BF02533722)
33. Minchin, P. R. 1987 Simulation of multidimensional community patterns: towards a comprehensive model. Vegetation 71, 145-156.
34. Moore, C. G. 1999 Aedes albopictus in the United States: current status and prospects for further spread. J. Am. Mosq. Control Assoc. 15, 221-227.
35. Mori, A., Oda, T. & Wada, Y. 1981 Studies on the egg diapause and overwintering of Aedes albopictus in Nagasaki. Trop. Med. 23, 79-90.
36. Mousson, L., Dauga, C., Garrigues, T., Schaffner, F., Vazeille, M. & Failoux, A. B. 2005 Phylogeography of Aedes (Stegomyia) aegypti (L.) and Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae) based on mito-chondrial DNA variations. Genet. Res. 86, 1-11. (doi:10.1017/S0016672305007627) (Pubitemid 41430670)
37. Nelson, D. R. & Blomquist, R. J. 1995 Insect waxes. In Waxes: chemistry and molecular biology and functions (ed. R. J. Hamilton), pp. 1-90. Dundee, UK: The Oily Press.
38. Pavelka, J., Shimada, K. & Kostal, V. 2003 TIMELESS: a link between fly's circadian and photoperiodic clocks? Eur. J. Entomol. 100, 255-265.
39. Rezende, G. L., Martins, A. J., Gentile, C., Farnesi, L. C., Pelajo-Machado, M., Peixoto, A. A. & Valle, D. 2008 Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev. Biol. 8, 82. (doi:10.1186/1471-213X-8-82)
40. Ribeiro, J. M. C., Arca, B., Lombardo, F., Calvo, E., Phan, V. M., Chandra, P. K. & Wikel, S. K. 2007 An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 8, (doi:10.1186/ 1471-2164-8-6)
41. Rinehart, J. P., Li, A. L., Yocum, G. D., Robich, R. M., Hayward, S. A. L. & Denlinger, D. L. 2007 Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proc. Natl Acad. Sci. USA 104, 11 130-11 137. (doi:10.1073/pnas.0703538104) (Pubitemid 47175106)
42. Scholte, E. J., Dijkstra, E., Blok, H., De Vries, A., Takken, W., Hofhuis, A., Koopmans, M., De Boer, A. & Reusken, C. B. E. M. 2008 Accidental importation of the mosquito Aedes albopictus into the Netherlands: a survey of mosquito distribution and the presence of dengue virus. Med. Vet. Entomol. 22, 352-358. (doi:10.1111/j.1365-2915.2008.00763.x)
43. Sota, T. & Mogi, M. 1992 Survival time and resistance to desiccation of diapause and nondiapause eggs of temperate Aedes (Stegomyia) mosquitoes. Entomol. Exp. Appl. 63, 155-161. (doi:10.1007/BF00343575)
44. Sprenger, D. & Wuithiranyagool, T. 1986 The discovery and distribution of Aedes albopictus in Harris County, Texas. J. Am. Mosq. Control Assoc. 2, 217-219.
45. Syrova, Z., Dolezel, D., Saumann, I. & Hodkova, M. 2003 Photoperiodic regulation of diapause in linden bugs: are period and clock genes involved? Cell. Mol. Life Sci. 60, 2510-2515. (doi:10.1007/s00018-003-3227-0) (Pubitemid 37487268)
46. Tauber, M. J., Tauber, C. A. & Masaki, S. 1986 Seasonal adaptations of insects. New York, NY: Oxford University Press.
47. Telford, A. D. 1957 The pasture Aedes of central and northern California. The egg stage: gross embryology and resistance to desiccation. Ann. Entomol. Soc. Am. 56, 537-543.
48. Turell, M. J., O'Guinn, M. L., Dohm, D. J. & Jones, J. W. 2001 Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J. Med. Entomol. 38, 130-134. (doi:10.1603/0022-2585-38.2.130)
49. Urbanski, J., Aruda, A. & Armbruster, P. In press. A tran-scriptional element of the diapause program in the Asian tiger mosquito, Aedes albopictus, identified by sup-pressive subtractive hybridization. J. Insect Physiol. (doi:10.1016/j.jinsphys.2010.03.008)
50. Van Handel, E. 1985 Rapid determination of total lipids in mosquitoes. J. Am. Mosq. Control Assoc. 1, 302-304.
51. Vaz, A. H., Blomquist, G. J. & Reitz, R. C. 1988 Characterization of the fatty acyl elongation reactions involved in hydrocarbon biosynthesis in the housefly, Musca domestica L. Insect Biochem. 18, 177-184. (doi:10.1016/0020- 1790(88)90022-4)
52. Wang, R. L. 1966 Observations on the influence of photo-period on egg diapause in Aedes albopictus Skuse. Acta Entomol. Sinica 15, 75-77.
53. Warwick, R. M., Clarke, K. R. & Suharnso 1990 A statistical analysis of coral community responses to the 1982-1983 El Niño in the Thousand Islands, Indonesia. Coral Reefs 8, 171-179. (doi:10.1007/BF00265008)
54. Wharton, G. W. 1985 Water balance of insects. In Comprehensive insect physiology, biochemistry, and pharmacology, vol. 4 (eds G. A. Kerkut & L. I. Gilbert), pp. 565-603. Oxford, UK: Pergamon Press.
55. Whitehead, A. & Crawford, D. L. 2005 Variation in tissue-specific gene expression among natural populations. Genome Biol. 6, R13. (doi:10.1186/gb-2005-6-2-r13)
56. Woods, H. A. 2005 Oxygen and water flux across eggshells of Manduca sexta. J. Exp. Biol. 208, 1297-1308. (doi:10.1242/jeb.01525) (Pubitemid 40564564)
57. Yoder, J. A. & Denlinger, D. L. 1991a Water balance in flesh fly pupae and water vapour absorption associated with diapause. J. Exp. Biol. 157, 273-286.
58. Yoder, J. A. & Denlinger, D. L. 1991b A comparison of the water balance characteristics of temperate and tropical fly pupae. Physiol. Entomol. 16, 375-380. (doi:10.1111/ j.1365-3032.1991.tb00575.x)
59. Yoder, J. A., Denlinger, D. L., Dennis, M. W. & Kolattukudy, P. E. 1992 Enhancement of diapausing flesh fly puparia with additional hydrocarbons and evidence for alkane biosynthesis by a decarbonylation mechanism. Insect Biochem. Mol. Biol. 22, 237-243. (doi:10.1016/0965-1748(92)90060-R)
60. Yoder, J. A., Blomquist, G. J. & Denlinger, D. L. 1995 Hydrocarbon profiles from puparia of diapausing and nondiapausing flesh flies (Sarcophaga crassipalpis) reflect quantitative rather than qualitative differences. Arch. Insect Biochem. Physiol. 28, 377-385. (doi:10.1002/arch. 940280407)