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. 1996 Jul;9(3):301–320. doi: 10.1128/cmr.9.3.301

Genetic variation in arthropod vectors of disease-causing organisms: obstacles and opportunities.

R H Gooding 1
PMCID: PMC172895  PMID: 8809462

Abstract

An overview of the genetic variation in arthropods that transmit pathogens to vertebrates is presented, emphasizing the genetics of vector-pathogen relationships and the biochemical genetics of vectors. Vector-pathogen interactions are reviewed briefly as a prelude to a discussion of the genetics of susceptibility and refractoriness in vectors. Susceptibility to pathogens is controlled by maternally inherited factors, sex-linked dominant alleles, and dominant and recessive autosomal genes. There is widespread interpopulation (including intercolony) and temporal variation in susceptibility to pathogens. The amount of biochemical genetic variation in vectors is similar to that found in other invertebrates. However, the amount varies widely among species, among populations within species, and temporally within populations. Biochemical genetic studies show that there is considerable genetic structuring of many vectors at the local, regional, and global levels. It is argued that genetic variation in vectors is critical in understanding vector-pathogen interactions and that genetic variation in vectors creates both obstacles to and opportunities for application of genetic techniques to the control of vectors.

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Selected References

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  1. Al-Mashhadani H. M., Davidson G., Curtis C. F. A genetic study of the susceptibility of Anopheles gambiae to Plasmodium berghei. Trans R Soc Trop Med Hyg. 1980;74(5):585–594. doi: 10.1016/0035-9203(80)90146-7. [DOI] [PubMed] [Google Scholar]
  2. Beaman J. R., Turell M. J. Transmission of Venezuelan equine encephalomyelitis virus by strains of Aedes albopictus (Diptera: Culicidae) collected in North and South America. J Med Entomol. 1991 Jan;28(1):161–164. doi: 10.1093/jmedent/28.1.161. [DOI] [PubMed] [Google Scholar]
  3. Beard C. B., Mason P. W., Aksoy S., Tesh R. B., Richards F. F. Transformation of an insect symbiont and expression of a foreign gene in the Chagas' disease vector Rhodnius prolixus. Am J Trop Med Hyg. 1992 Feb;46(2):195–200. doi: 10.4269/ajtmh.1992.46.195. [DOI] [PubMed] [Google Scholar]
  4. Beard C. B., O'Neill S. L., Tesh R. B., Richards F. F., Aksoy S. Modification of arthropod vector competence via symbiotic bacteria. Parasitol Today. 1993 May;9(5):179–183. doi: 10.1016/0169-4758(93)90142-3. [DOI] [PubMed] [Google Scholar]
  5. Berry W. J., Rowley W. A., Christensen B. M. Influence of developing Brugia pahangi on spontaneous flight activity of Aedes aegypti (Diptera: Culicidae). J Med Entomol. 1986 Jul 28;23(4):441–445. doi: 10.1093/jmedent/23.4.441. [DOI] [PubMed] [Google Scholar]
  6. Berry W. J., Rowley W. A., Christensen B. M. Influence of developing Dirofilaria immitis on the spontaneous flight activity of Aedes aegypti (Diptera: Culicidae). J Med Entomol. 1987 Nov;24(6):699–701. doi: 10.1093/jmedent/24.6.699. [DOI] [PubMed] [Google Scholar]
  7. Besansky N. J., Finnerty V., Collins F. H. Molecular perspectives on the genetics of mosquitoes. Adv Genet. 1992;30:123–184. doi: 10.1016/s0065-2660(08)60320-x. [DOI] [PubMed] [Google Scholar]
  8. Black W. C., 4th, Ferrari J. A., Rai K. S., Sprenger D. Breeding structure of a colonising species: Aedes albopictus (Skuse) in the United States. Heredity (Edinb) 1988 Apr;60(Pt 2):173–181. doi: 10.1038/hdy.1988.29. [DOI] [PubMed] [Google Scholar]
  9. Borovsky D., Schlein Y. Trypsin and chymotrypsin-like enzymes of the sandfly Phlebotomus papatasi infected with Leishmania and their possible role in vector competence. Med Vet Entomol. 1987 Jul;1(3):235–242. doi: 10.1111/j.1365-2915.1987.tb00349.x. [DOI] [PubMed] [Google Scholar]
  10. Bosio C. F., Thomas R. E., Grimstad P. R., Rai K. S. Variation in the efficiency of vertical transmission of dengue-1 virus by strains of Aedes albopictus (Diptera: Culicidae). J Med Entomol. 1992 Nov;29(6):985–989. doi: 10.1093/jmedent/29.6.985. [DOI] [PubMed] [Google Scholar]
  11. CRAIG G. B., Jr, HICKEY W. A., VANDEHEY R. C. An inherited male-producing factor in Aedes aegypti. Science. 1960 Dec 23;132(3443):1887–1889. doi: 10.1126/science.132.3443.1887. [DOI] [PubMed] [Google Scholar]
  12. Caillard T., Tibayrenc M., Le Pont F., Dujardin J. P., Desjeux P., Ayala F. J. Diagnosis by isozyme methods of two cryptic species, Psychodopygus carrerai and P. yucumensis (Diptera: Psychodidae). J Med Entomol. 1986 Sep 19;23(5):489–492. doi: 10.1093/jmedent/23.5.489. [DOI] [PubMed] [Google Scholar]
  13. Chan A. S., Rodríguez M. H., Torres J. A., Rodríguez M. del C., Villarreal C. Susceptibility of three laboratory strains of Anopheles albimanus (Diptera: Culicidae) to coindigenous Plasmodium vivax in southern Mexico. J Med Entomol. 1994 May;31(3):400–403. doi: 10.1093/jmedent/31.3.400. [DOI] [PubMed] [Google Scholar]
  14. Coetzee M., Hunt R. H., Braack L. E. Enzyme variation at the aspartate aminotransferase locus in members of the Anopheles gambiae complex (Diptera: Culicidae). J Med Entomol. 1993 Mar;30(2):303–308. doi: 10.1093/jmedent/30.2.303. [DOI] [PubMed] [Google Scholar]
  15. Collins F. H., Sakai R. K., Vernick K. D., Paskewitz S., Seeley D. C., Miller L. H., Collins W. E., Campbell C. C., Gwadz R. W. Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science. 1986 Oct 31;234(4776):607–610. doi: 10.1126/science.3532325. [DOI] [PubMed] [Google Scholar]
  16. Coluzzi M., Cancrini G. Genetica della suscettibilità di Aedes aegypti a Dirofilaria repens. Parassitologia. 1974 Aug-Dec;16(2-3):239–256. [PubMed] [Google Scholar]
  17. 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(5):483–497. doi: 10.1016/0035-9203(79)90036-1. [DOI] [PubMed] [Google Scholar]
  18. Crampton J., Morris A., Lycett G., Warren A., Eggleston P. Transgenic mosquitoes: a future vector control strategy? Parasitol Today. 1990 Feb;6(2):31–36. doi: 10.1016/0169-4758(90)90057-b. [DOI] [PubMed] [Google Scholar]
  19. Crews-Oyen A. E., Kumar V., Collins F. H. Association of two esterase genes, a chromosomal inversion, and susceptibility to Plasmodium cynomolgi in the African malaria vector Anopheles gambiae. Am J Trop Med Hyg. 1993 Sep;49(3):341–347. doi: 10.4269/ajtmh.1993.49.341. [DOI] [PubMed] [Google Scholar]
  20. DeFoliart G. R., Grimstad P. R., Watts D. M. Advances in mosquito-borne arbovirus/vector research. Annu Rev Entomol. 1987;32:479–505. doi: 10.1146/annurev.en.32.010187.002403. [DOI] [PubMed] [Google Scholar]
  21. Distelmans W., Makumyaviri A. M., D'Haeseleer F., Claes Y., Le Ray D., Gooding R. H. Influence of the salmon mutant of Glossina morsitans morsitans on the susceptibility to infection with Trypanosoma congolense. Acta Trop. 1985 Jun;42(2):143–148. [PubMed] [Google Scholar]
  22. Duhrkopf R. E., Trpis M. The degree of susceptibility and levels of infection in ten different strains of Aedes polynesiensis Marks infected with subperiodic Brugia malayi and Brugia pahangi. Am J Trop Med Hyg. 1980 Sep;29(5):815–819. doi: 10.4269/ajtmh.1980.29.815. [DOI] [PubMed] [Google Scholar]
  23. Dujardin J. P., Tibayrenc M. Etude de 11 enzymes et données de génétique formelle pour 19 loci enzymatiques chez Triatoma infestans (Hemiptera: Reduviidae). Ann Soc Belg Med Trop. 1985 Sep;65(3):271–280. [PubMed] [Google Scholar]
  24. Eldridge B. F., Munstermann L. E., Craig G. B., Jr Enzyme variation in some mosquito species related to Aedes (Ochlerotatus) stimulans (Diptera: Culicidae). J Med Entomol. 1986 Jul 28;23(4):423–428. doi: 10.1093/jmedent/23.4.423. [DOI] [PubMed] [Google Scholar]
  25. Elsen P., Roelants P., De Lil E., Dujardin J. P., Le Ray D., Claes Y. Cytogenetic and isozymic comparisons of two laboratory lines of Glossina palpalis gambiensis. Ann Trop Med Parasitol. 1994 Oct;88(5):511–522. doi: 10.1080/00034983.1994.11812898. [DOI] [PubMed] [Google Scholar]
  26. Faran M. E., Turell M. J., Romoser W. S., Routier R. G., Gibbs P. H., Cannon T. L., Bailey C. L. Reduced survival of adult Culex pipiens infected with Rift Valley fever virus. Am J Trop Med Hyg. 1987 Sep;37(2):403–409. doi: 10.4269/ajtmh.1987.37.403. [DOI] [PubMed] [Google Scholar]
  27. Farid H. A., Gad A. M., Spielman A. Genetic similarity among Egyptian populations of Culex pipiens (Diptera: Culicidae). J Med Entomol. 1991 Mar;28(2):198–204. doi: 10.1093/jmedent/28.2.198. [DOI] [PubMed] [Google Scholar]
  28. Feldmann A. M., Billingsley P. F., Savelkoul E. Bloodmeal digestion by strains of Anopheles stephensi liston (Diptera: Culicidae) of differing susceptibility to Plasmodium falciparum. Parasitology. 1990 Oct;101(Pt 2):193–200. doi: 10.1017/s003118200006323x. [DOI] [PubMed] [Google Scholar]
  29. Feldmann A. M., Ponnudurai T. Selection of Anopheles stephensi for refractoriness and susceptibility to Plasmodium falciparum. Med Vet Entomol. 1989 Jan;3(1):41–52. doi: 10.1111/j.1365-2915.1989.tb00473.x. [DOI] [PubMed] [Google Scholar]
  30. GILLIES M. T. SELECTION FOR HOST PREFERENCE IN ANOPHELES GAMBIAE. Nature. 1964 Aug 22;203:852–854. doi: 10.1038/203852a0. [DOI] [PubMed] [Google Scholar]
  31. Gale K. R., Crampton J. M. Use of a male-specific DNA probe to distinguish female mosquitoes of the Anopheles gambiae species complex. Med Vet Entomol. 1988 Jan;2(1):77–79. doi: 10.1111/j.1365-2915.1988.tb00051.x. [DOI] [PubMed] [Google Scholar]
  32. Gooding R. H. Genetic variation in tsetse flies and implications for trypanosomiasis. Parasitol Today. 1992 Mar;8(3):92–95. doi: 10.1016/0169-4758(92)90246-x. [DOI] [PubMed] [Google Scholar]
  33. Gooding R. H. Genetics of two populations of Glossina morsitans centralis (Diptera: Glossinidae) from Zambia. Acta Trop. 1989 Jan;46(1):17–22. doi: 10.1016/0001-706x(89)90012-0. [DOI] [PubMed] [Google Scholar]
  34. Gooding R. H., Mbise S., Macha P., Rolseth B. M. Genetic variation in a Tanzanian population of Glossina swynnertoni (Diptera: Glossinidae). J Med Entomol. 1993 Mar;30(2):489–492. doi: 10.1093/jmedent/30.2.489. [DOI] [PubMed] [Google Scholar]
  35. Gooding R. H., Moloo S. K. Genetics of two colonies of Glossina pallidipes originating from allopatric populations in Kenya. Med Vet Entomol. 1994 Apr;8(2):133–136. doi: 10.1111/j.1365-2915.1994.tb00152.x. [DOI] [PubMed] [Google Scholar]
  36. Gooding R. H., Moloo S. K., Rolseth B. M. Genetic variation in Glossina brevipalpis, G.longipennis and G.pallidipes, and the phenetic relationships of Glossina species. Med Vet Entomol. 1991 Apr;5(2):165–173. doi: 10.1111/j.1365-2915.1991.tb00537.x. [DOI] [PubMed] [Google Scholar]
  37. Graves P. M., Curtis C. F. A cage replacement experiment involving introduction of genes for refractoriness to Plasmodium yoelii nigeriensis into a population of Anopheles gambiae (Diptera: Culicidae). J Med Entomol. 1982 Mar 24;19(2):127–133. doi: 10.1093/jmedent/19.2.127. [DOI] [PubMed] [Google Scholar]
  38. Graves P. M., Curtis C. F. Susceptibility of Anopheles gambiae to Plasmodium yoelii nigeriensis and Plasmodium falciparum. Ann Trop Med Parasitol. 1982 Dec;76(6):633–639. [PubMed] [Google Scholar]
  39. Green C. A., Gass R. F., Munstermann L. E., Baimai V. Population-genetic evidence for two species in Anopheles minimus in Thailand. Med Vet Entomol. 1990 Jan;4(1):25–34. doi: 10.1111/j.1365-2915.1990.tb00256.x. [DOI] [PubMed] [Google Scholar]
  40. Grimstad P. R., Craig G. B., Jr, Ross Q. E., Yuill T. M. Aedes triseriatus and LA crosse virus: geographic variation in vector susceptibility and ability to transmit. Am J Trop Med Hyg. 1977 Sep;26(5 Pt 1):990–996. doi: 10.4269/ajtmh.1977.26.990. [DOI] [PubMed] [Google Scholar]
  41. Grimstad P. R., Ross Q. E., Craig G. B., Jr Aedes triseriatus (Diptera: Culicidae) and La Crosse virus. II. Modification of mosquito feeding behavior by virus infection. J Med Entomol. 1980 Jan 31;17(1):1–7. doi: 10.1093/jmedent/17.1.1. [DOI] [PubMed] [Google Scholar]
  42. Gubler D. J., Rosen L. Variation among geographic strains of Aedes albopictus in susceptibility to infection with dengue viruses. Am J Trop Med Hyg. 1976 Mar;25(2):318–325. doi: 10.4269/ajtmh.1976.25.318. [DOI] [PubMed] [Google Scholar]
  43. Gwadz R. W. Genetic approaches to malaria control: how long the road? Am J Trop Med Hyg. 1994;50(6 Suppl):116–125. doi: 10.4269/ajtmh.1994.50.116. [DOI] [PubMed] [Google Scholar]
  44. Hanson S. M., Mutebi J. P., Craig G. B., Jr, Novak R. J. Reducing the overwintering ability of Aedes albopictus by male release. J Am Mosq Control Assoc. 1993 Mar;9(1):78–83. [PubMed] [Google Scholar]
  45. Hardy J. L., Apperson G., Asman S. M., Reeves W. C. Selection of a strain of Culex tarsalis highly resistant to infection following ingestion of western equine encephalomyelitis virus. Am J Trop Med Hyg. 1978 Mar;27(2 Pt 1):313–321. doi: 10.4269/ajtmh.1978.27.313. [DOI] [PubMed] [Google Scholar]
  46. Hardy J. L., Houk E. J., Kramer L. D., Reeves W. C. Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol. 1983;28:229–262. doi: 10.1146/annurev.en.28.010183.001305. [DOI] [PubMed] [Google Scholar]
  47. Hardy J. L., Meyer R. P., Presser S. B., Milby M. M. Temporal variations in the susceptibility of a semi-isolated population of Culex tarsalis to peroral infection with western equine encephalomyelitis and St. Louis encephalitis viruses. Am J Trop Med Hyg. 1990 May;42(5):500–511. doi: 10.4269/ajtmh.1990.42.500. [DOI] [PubMed] [Google Scholar]
  48. Harrington M. A., Hacker C. S., Cheng M. L., Ferrell R. E. Genetic variation in an urban population of Aedes aegypti (Diptera: Culicidae). J Med Entomol. 1984 Nov 29;21(6):706–710. doi: 10.1093/jmedent/21.6.706. [DOI] [PubMed] [Google Scholar]
  49. Harry M., Galindez I., Cariou M. L. Isozyme variability and differentiation between Rhodnius prolixus, R.robustus and R.pictipes, vectors of Chagas disease in Venezuela. Med Vet Entomol. 1992 Jan;6(1):37–43. doi: 10.1111/j.1365-2915.1992.tb00032.x. [DOI] [PubMed] [Google Scholar]
  50. Hartberg W. K., Meeks C. K., Williams K. R. A model for polygenic inheritance of abdominal tergal scale pattern in Aedes aegypti. J Am Mosq Control Assoc. 1986 Dec;2(4):490–502. [PubMed] [Google Scholar]
  51. Hii J. L., Chew M., Sang V. Y., Munstermann L. E., Tan S. G., Panyim S., Yasothornsrikul S. Population genetic analysis of host seeking and resting behaviors in the malaria vector, Anopheles balabacensis (Diptera: Culicidae). J Med Entomol. 1991 Sep;28(5):675–684. doi: 10.1093/jmedent/28.5.675. [DOI] [PubMed] [Google Scholar]
  52. Hilburn L. R., Sattler P. W. Electrophoretically detectable protein variation in natural populations of the lone star tick, Amblyomma americanum (Acari: Ixodidae). Heredity (Edinb) 1986 Aug;57(Pt 1):67–74. doi: 10.1038/hdy.1986.88. [DOI] [PubMed] [Google Scholar]
  53. Hunt R. H., Coetzee M. A parasitological, cytogenetic and biochemical study of Anopheles gambiae (Diptera: Culicidae) from the People's Republic of Congo. S Afr Med J. 1989 Oct 7;76(7):362–364. [PubMed] [Google Scholar]
  54. Janssen J. A., Wijers D. J. Trypanosoma simiae at the Kenya coast. A correlation between virulence and the transmitting species of Glossina. Ann Trop Med Parasitol. 1974 Mar;68(1):5–19. doi: 10.1080/00034983.1974.11686919. [DOI] [PubMed] [Google Scholar]
  55. Jones R. H., Foster N. M. Relevance of laboratory colonies of the vector in arbovirus research--Culicoides variipennis and bluetongue. Am J Trop Med Hyg. 1978 Jan;27(1 Pt 1):168–177. doi: 10.4269/ajtmh.1978.27.168. [DOI] [PubMed] [Google Scholar]
  56. Kambhampati S., Black W. C., 4th, Rai K. S., Sprenger D. Temporal variation in genetic structure of a colonising species: Aedes albopictus in the United States. Heredity (Edinb) 1990 Apr;64(Pt 2):281–287. doi: 10.1038/hdy.1990.34. [DOI] [PubMed] [Google Scholar]
  57. Kambhampati S., Rai K. S. Mitochondrial DNA variation within and among populations of the mosquito Aedes albopictus. Genome. 1991 Apr;34(2):288–292. doi: 10.1139/g91-046. [DOI] [PubMed] [Google Scholar]
  58. Kambhampati S., Rai K. S., Verleye D. M. Frequencies of mitochondrial DNA haplotypes in laboratory cage populations of the mosquito, Aedes albopictus. Genetics. 1992 Sep;132(1):205–209. doi: 10.1093/genetics/132.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Kassem H. A., Fryauff D. J., Shehata M. G., el Sawaf B. M. Enzyme polymorphism and genetic variability of one colonized and several field populations of Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol. 1993 Mar;30(2):407–413. doi: 10.1093/jmedent/30.2.407. [DOI] [PubMed] [Google Scholar]
  60. Kilama W. L., Craig G. B., Jr Monofactorial inheritance of susceptibility to Plasmodium Gallinaceum in Aedes aegypti. Ann Trop Med Parasitol. 1969 Dec;63(4):419–432. doi: 10.1080/00034983.1969.11686645. [DOI] [PubMed] [Google Scholar]
  61. Kramer L. D., Hardy J. L., Houk E. J., Presser S. B. Characterization of the mesenteronal infection with Western equine encephalomyelitis virus in an incompetent strain of Culex tarsalis. Am J Trop Med Hyg. 1989 Aug;41(2):241–250. doi: 10.4269/ajtmh.1989.41.241. [DOI] [PubMed] [Google Scholar]
  62. Kramer L. D., Hardy J. L., Presser S. B., Houk E. J. Dissemination barriers for western equine encephalomyelitis virus in Culex tarsalis infected after ingestion of low viral doses. Am J Trop Med Hyg. 1981 Jan;30(1):190–197. doi: 10.4269/ajtmh.1981.30.190. [DOI] [PubMed] [Google Scholar]
  63. Kreutzer R. D., Palau M. T., Morales A., Ferro C., Feliciangeli D., Young D. G. Genetic relationships among phlebotomine sand flies (Diptera: Psychodidae) in the verrucarum species group. J Med Entomol. 1990 Jan;27(1):1–8. doi: 10.1093/jmedent/27.1.1. [DOI] [PubMed] [Google Scholar]
  64. Lanzaro G. C., Ostrovska K., Herrero M. V., Lawyer P. G., Warburg A. Lutzomyia longipalpis is a species complex: genetic divergence and interspecific hybrid sterility among three populations. Am J Trop Med Hyg. 1993 Jun;48(6):839–847. doi: 10.4269/ajtmh.1993.48.839. [DOI] [PubMed] [Google Scholar]
  65. Lehane M. J., Msangi A. R. Lectin and peritrophic membrane development in the gut of Glossina m.morsitans and a discussion of their role in protecting the fly against trypanosome infection. Med Vet Entomol. 1991 Oct;5(4):495–501. doi: 10.1111/j.1365-2915.1991.tb00578.x. [DOI] [PubMed] [Google Scholar]
  66. Lorenz L., Beaty B. J., Aitken T. H., Wallis G. P., Tabachnick W. J. The effect of colonization upon aedes aegypti susceptibility to oral infection with yellow fever virus. Am J Trop Med Hyg. 1984 Jul;33(4):690–694. doi: 10.4269/ajtmh.1984.33.690. [DOI] [PubMed] [Google Scholar]
  67. MACDONALD W. W., RAMACHANDRAN C. P. THE INFLUENCE OF THE GENE FM (FILARIAL SUSCEPTIBILITY, BRUGIA MALAYI) ON THE SUSCEPTIBILITY OF AEDES AEGYPTI TO SEVEN STRAINS OF BRUGIA, WUCHERERIA AND DIROFILARIA. Ann Trop Med Parasitol. 1965 Mar;59:64–73. doi: 10.1080/00034983.1965.11686284. [DOI] [PubMed] [Google Scholar]
  68. Magnin M., Pasteur N., Raymond M. Multiple incompatibilities within populations of Culex pipiens L. in southern France. Genetica. 1987 Oct 15;74(2):125–130. doi: 10.1007/BF00055223. [DOI] [PubMed] [Google Scholar]
  69. Mani G. S., Cook L. M., Marvdashti R. What can be learnt about selection from gene frequency distribution? Genetics. 1986 Nov;114(3):971–982. doi: 10.1093/genetics/114.3.971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Matthews T. C., Craig G. B., Jr Heterozygosity in inbred strains of the tree-hole mosquito Aedes triseriatus. Biochem Genet. 1987 Oct;25(9-10):647–655. doi: 10.1007/BF00556209. [DOI] [PubMed] [Google Scholar]
  71. Matthews T. C., Craig G. B., Jr Isozyme polymorphisms maintained by lethal loci in inbred strains of Aedes triseriatus. J Hered. 1989 Jan-Feb;80(1):53–57. doi: 10.1093/oxfordjournals.jhered.a110789. [DOI] [PubMed] [Google Scholar]
  72. Matthews T. C. Population genetics of the tree hole mosquito Aedes triseriatus: no correlation between Est-6 and larval habitat. Heredity (Edinb) 1984 Feb;52(Pt 1):133–139. doi: 10.1038/hdy.1984.13. [DOI] [PubMed] [Google Scholar]
  73. Maudlin I., Dukes P. Extrachromosomal inheritance of susceptibility to trypanosome infection in tsetse flies. I. Selection of susceptible and refractory lines of Glossina morsitans morsitans. Ann Trop Med Parasitol. 1985 Jun;79(3):317–324. doi: 10.1080/00034983.1985.11811925. [DOI] [PubMed] [Google Scholar]
  74. Maudlin I., Dukes P., Luckins A. G., Hudson K. M. Extrachromosomal inheritance of susceptibility to trypanosome infection in tsetse flies. II. Susceptibility of selected lines of Glossina morsitans morsitans to different stocks and species of trypanosome. Ann Trop Med Parasitol. 1986 Feb;80(1):97–105. doi: 10.1080/00034983.1986.11811987. [DOI] [PubMed] [Google Scholar]
  75. Maudlin I., Welburn S. C. The role of lectins and trypanosome genotype in the maturation of midgut infections in Glossina morsitans. Trop Med Parasitol. 1988 Mar;39(1):56–58. [PubMed] [Google Scholar]
  76. McGreevy P. B., McClelland G. A., Lavoipierre M. M. Inheritance of susceptibility to Dirofilaria immitis infection in Aedes aegypti. Ann Trop Med Parasitol. 1974 Mar;68(1):97–109. doi: 10.1080/00034983.1974.11686929. [DOI] [PubMed] [Google Scholar]
  77. Mebrahtu Y., Beach R. F., Hendricks L. D., Oster C. N. Isozyme variation in Simulium (Edwardsellum) damnosum s.l. (Diptera: Simuliidae) from Kenya. J Am Mosq Control Assoc. 1987 Jun;3(2):196–200. [PubMed] [Google Scholar]
  78. Mebrahtu Y., Beach R. F., Khamala C. P., Hendricks L. D. Characterization of Simulium (Edwardsellum) damnosum s.l. populations from six river systems in Kenya by cellulose acetate electrophoresis. Trans R Soc Trop Med Hyg. 1986;80(6):914–922. doi: 10.1016/0035-9203(86)90258-0. [DOI] [PubMed] [Google Scholar]
  79. Mecham J. O., Nunamaker R. A. Complex interactions between vectors and pathogens: Culicoides variipennis sonorensis (Diptera: Ceratopogonidae) infection rates with bluetongue viruses. J Med Entomol. 1994 Nov;31(6):903–907. doi: 10.1093/jmedent/31.6.903. [DOI] [PubMed] [Google Scholar]
  80. Meek S. R., Macdonald W. W. Studies on the inheritance of susceptibility to infection with Brugia pahangi and Wuchereria bancrofti in the Aedes scutellaris group of mosquitoes. Ann Trop Med Parasitol. 1982 Jun;76(3):347–354. doi: 10.1080/00034983.1982.11687551. [DOI] [PubMed] [Google Scholar]
  81. Miller B. R., Mitchell C. J. Genetic selection of a flavivirus-refractory strain of the yellow fever mosquito Aedes aegypti. Am J Trop Med Hyg. 1991 Oct;45(4):399–407. doi: 10.4269/ajtmh.1991.45.399. [DOI] [PubMed] [Google Scholar]
  82. Moloo S. K. A comparison of susceptibility of two allopatric populations of Glossina pallidipes for stocks of Trypanosoma congolense. Med Vet Entomol. 1993 Oct;7(4):369–372. doi: 10.1111/j.1365-2915.1993.tb00707.x. [DOI] [PubMed] [Google Scholar]
  83. Munstermann L. E., Marchi A. Cytogenetic and isozyme profile of Sabethes cyaneus: a mosquito of the neotropical canopy. J Hered. 1986 Jul-Aug;77(4):241–248. doi: 10.1093/oxfordjournals.jhered.a110229. [DOI] [PubMed] [Google Scholar]
  84. Narang S. K., Klein T. A., Perera O. P., Lima J. B., Tang A. T. Genetic evidence for the existence of cryptic species in the Anopheles albitarsis complex in Brazil: allozymes and mitochondrial DNA restriction fragment length polymorphisms. Biochem Genet. 1993 Feb;31(1-2):97–112. doi: 10.1007/BF02399823. [DOI] [PubMed] [Google Scholar]
  85. Narang S. K., Seawright J. A., Kaiser P. E. Evidence for microgeographic genetic subdivision of Anopheles quadrimaculatus species C. J Am Mosq Control Assoc. 1990 Jun;6(2):179–187. [PubMed] [Google Scholar]
  86. Narang S. K., Seawright J. A., Suarez M. F. Genetic structure of natural populations of Anopheles albimanus in Colombia. J Am Mosq Control Assoc. 1991 Sep;7(3):437–445. [PubMed] [Google Scholar]
  87. Nayar J. K., Knight J. W., Kaiser P. E., Seawright J. A., Narang S. K. Comparative susceptibility of species A, B and C of Anopheles quadrimaculatus complex to infection with subperiodic Brugia malayi and Brugia pahangi (Nematoda: Filarioidea). J Am Mosq Control Assoc. 1992 Mar;8(1):61–64. [PubMed] [Google Scholar]
  88. Nayar J. K., Knight J. W., Vickery A. C. Intracellular melanization in the mosquito Anopheles quadrimaculatus (Diptera: Culicidae) against the filarial nematodes, Brugia spp. (Nematoda: Filarioidea). J Med Entomol. 1989 May;26(3):159–166. doi: 10.1093/jmedent/26.3.159. [DOI] [PubMed] [Google Scholar]
  89. Nesbitt S. A., Gooding R. H., Rolseth B. M. Genetic variation in two field populations and a laboratory colony of Glossina pallidipes (Diptera: Glossinidae). J Med Entomol. 1990 Jul;27(4):586–591. doi: 10.1093/jmedent/27.4.586. [DOI] [PubMed] [Google Scholar]
  90. O'Neill S. L., Paterson H. E. Crossing type variability associated with cytoplasmic incompatibility in Australian populations of the mosquito Culex quinquefasciatus Say. Med Vet Entomol. 1992 Jul;6(3):209–216. doi: 10.1111/j.1365-2915.1992.tb00608.x. [DOI] [PubMed] [Google Scholar]
  91. Obiamiwe B. A. The influence of the gene sb in Culex pipiens on the development of sub-periodic Brugia malayi and Wuchereria bancrofti. Ann Trop Med Parasitol. 1977 Dec;71(4):487–490. [PubMed] [Google Scholar]
  92. Osir E. O., Imbuga M. O., Onyango P. Inhibition of Glossina morsitans midgut trypsin activity by D-glucosamine. Parasitol Res. 1993;79(2):93–97. doi: 10.1007/BF00932252. [DOI] [PubMed] [Google Scholar]
  93. Pal R., LaChance L. E. The operational feasibility of genetic methods for control of insects of medical and veterinary importance. Annu Rev Entomol. 1974;19:269–291. doi: 10.1146/annurev.en.19.010174.001413. [DOI] [PubMed] [Google Scholar]
  94. Partono F. Studies of the susceptibility of Culex pipiens fatigans from non-endemic filarial areas to urban Wuchereria bancrofti. Ann Trop Med Parasitol. 1979 Feb;73(1):79–81. doi: 10.1080/00034983.1979.11687230. [DOI] [PubMed] [Google Scholar]
  95. Paskewitz S. M., Brown M. R., Lea A. O., Collins F. H. Ultrastructure of the encapsulation of Plasmodium cynomolgi (B strain) on the midgut of a refractory strain of Anopheles gambiae. J Parasitol. 1988 Jun;74(3):432–439. [PubMed] [Google Scholar]
  96. Paulson S. L., Grimstad P. R., Craig G. B., Jr Midgut and salivary gland barriers to La Crosse virus dissemination in mosquitoes of the Aedes triseriatus group. Med Vet Entomol. 1989 Apr;3(2):113–123. doi: 10.1111/j.1365-2915.1989.tb00485.x. [DOI] [PubMed] [Google Scholar]
  97. Paulson S. L., Grimstad P. R. Replication and dissemination of La Crosse virus in the competent vector Aedes triseriatus and the incompetent vector Aedes hendersoni and evidence for transovarial transmission by Aedes hendersoni (Diptera: Culicidae). J Med Entomol. 1989 Nov;26(6):602–609. doi: 10.1093/jmedent/26.6.602. [DOI] [PubMed] [Google Scholar]
  98. Pereira M. E., Andrade A. F., Ribeiro J. M. Lectins of distinct specificity in Rhodnius prolixus interact selectively with Trypanosoma cruzi. Science. 1981 Feb 6;211(4482):597–600. doi: 10.1126/science.7006082. [DOI] [PubMed] [Google Scholar]
  99. Procunier W. S. Cytological approaches to simuliid biosystematics in relation to the epidemiology and control of human onchocerciasis. Genome. 1989 Aug;32(4):559–569. doi: 10.1139/g89-483. [DOI] [PubMed] [Google Scholar]
  100. Pryor S. C., Daly J. Temporal variation in morphological and genetic characteristics within a hybrid population of Culex pipiens (Diptera: Culicidae). J Med Entomol. 1991 Jul;28(4):481–486. doi: 10.1093/jmedent/28.4.481. [DOI] [PubMed] [Google Scholar]
  101. Rai K. S. Genetics of Aedes albopictus. J Am Mosq Control Assoc. 1986 Dec;2(4):429–436. [PubMed] [Google Scholar]
  102. Ribeiro J. M., Vachereau A., Modi G. B., Tesh R. B. A novel vasodilatory peptide from the salivary glands of the sand fly Lutzomyia longipalpis. Science. 1989 Jan 13;243(4888):212–214. doi: 10.1126/science.2783496. [DOI] [PubMed] [Google Scholar]
  103. Rosen L., Lien J. C., Shroyer D. A., Baker R. H., Lu L. C. Experimental vertical transmission of Japanese encephalitis virus by Culex tritaeniorhynchus and other mosquitoes. Am J Trop Med Hyg. 1989 May;40(5):548–556. doi: 10.4269/ajtmh.1989.40.548. [DOI] [PubMed] [Google Scholar]
  104. Roush R. T., McKenzie J. A. Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol. 1987;32:361–380. doi: 10.1146/annurev.en.32.010187.002045. [DOI] [PubMed] [Google Scholar]
  105. Sattler P. W., Hilburn L. R., Davey R. B., George J. E., Rojas Avalos J. B. Genetic similarity and variability between natural populations and laboratory colonies of North American Boophilus (Acari: Ixodidae). J Parasitol. 1986 Feb;72(1):95–100. [PubMed] [Google Scholar]
  106. Schaub G. A. Does Trypanosoma cruzi stress its vectors? Parasitol Today. 1989 Jun;5(6):185–188. doi: 10.1016/0169-4758(89)90142-7. [DOI] [PubMed] [Google Scholar]
  107. Schaub G. A., Lösch P. Parasite/host-interrelationships of the trypanosomatids Trypanosoma cruzi and Blastocrithidia triatomae and the reduviid bug Triatoma infestans: influence of starvation of the bug. Ann Trop Med Parasitol. 1989 Jun;83(3):215–223. doi: 10.1080/00034983.1989.11812335. [DOI] [PubMed] [Google Scholar]
  108. Schaub G. A. The effects of trypanosomatids on insects. Adv Parasitol. 1992;31:255–319. doi: 10.1016/s0065-308x(08)60023-8. [DOI] [PubMed] [Google Scholar]
  109. Schlein Y., Romano H. Leishmania major and L. donovani: effects on proteolytic enzymes of Phlebotomus papatasi (Diptera, Psychodidae). Exp Parasitol. 1986 Dec;62(3):376–380. doi: 10.1016/0014-4894(86)90045-7. [DOI] [PubMed] [Google Scholar]
  110. Shroyer D. A. Aedes albopictus and arboviruses: a concise review of the literature. J Am Mosq Control Assoc. 1986 Dec;2(4):424–428. [PubMed] [Google Scholar]
  111. Stiles J. K., Ingram G. A., Wallbanks K. R., Molyneux D. H., Maudlin I., Welburn S. Identification of midgut trypanolysin and trypanoagglutinin in Glossina palpalis sspp. (Diptera: Glossinidae). Parasitology. 1990 Dec;101(Pt 3):369–376. doi: 10.1017/s003118200006056x. [DOI] [PubMed] [Google Scholar]
  112. Sulaiman I., Townson H. The genetic basis of susceptibility to infection with Dirofilaria immitis in Aedes aegypti. Ann Trop Med Parasitol. 1980 Dec;74(6):635–646. doi: 10.1080/00034983.1980.11687397. [DOI] [PubMed] [Google Scholar]
  113. Tabachnick W. J. Genetic control of oral susceptibility to infection of Culicoides variipennis with bluetongue virus. Am J Trop Med Hyg. 1991 Dec;45(6):666–671. doi: 10.4269/ajtmh.1991.45.666. [DOI] [PubMed] [Google Scholar]
  114. Tabachnick W. J. Genetic variation in laboratory and field populations of the vector of bluetongue virus, Culicoides variipennis (Diptera: Ceratopogonidae). J Med Entomol. 1990 Jan;27(1):24–30. doi: 10.1093/jmedent/27.1.24. [DOI] [PubMed] [Google Scholar]
  115. Tabachnick W. J. Microgeographic and temporal genetic variation in populations of the bluetongue virus vector Culicoides variipennis (Diptera: Ceratopogonidae). J Med Entomol. 1992 May;29(3):384–394. doi: 10.1093/jmedent/29.3.384. [DOI] [PubMed] [Google Scholar]
  116. Tabachnick W. J., Powell J. R. Genetic structure of the East African domestic populations of Aedes aegypti. Nature. 1978 Apr 6;272(5653):535–537. doi: 10.1038/272535a0. [DOI] [PubMed] [Google Scholar]
  117. Tabachnick W. J., Wallis G. P., Aitken T. H., Miller B. R., Amato G. D., Lorenz L., Powell J. R., Beaty B. J. Oral infection of Aedes aegypti with yellow fever virus: geographic variation and genetic considerations. Am J Trop Med Hyg. 1985 Nov;34(6):1219–1224. doi: 10.4269/ajtmh.1985.34.1219. [DOI] [PubMed] [Google Scholar]
  118. Terwedow H. A., Jr, Craig G. B., Jr Waltonella flexicauda: development controlled by a genetic factor in Aedes aegypti. Exp Parasitol. 1977 Apr;41(2):272–282. doi: 10.1016/0014-4894(77)90100-x. [DOI] [PubMed] [Google Scholar]
  119. Tesh R. B. Experimental studies on the transovarial transmission of Kunjin and San Angelo viruses in mosquitoes. Am J Trop Med Hyg. 1980 Jul;29(4):657–666. doi: 10.4269/ajtmh.1980.29.657. [DOI] [PubMed] [Google Scholar]
  120. Townson H., Chaithong U. Mosquito host influences on development of filariae. Ann Trop Med Parasitol. 1991 Feb;85(1):149–163. doi: 10.1080/00034983.1991.11812541. [DOI] [PubMed] [Google Scholar]
  121. Trpis M., Duhrkopf R. E., Parker K. L. Non-Mendelian inheritance of mosquito susceptibility to infection with Brugia malayi and Brugia pahangi. Science. 1981 Mar 27;211(4489):1435–1437. doi: 10.1126/science.7466401. [DOI] [PubMed] [Google Scholar]
  122. Turell M. J., Beaman J. R. Experimental transmission of Venezuelan equine encephalomyelitis virus by a strain of Aedes albopictus (Diptera: Culicidae) from New Orleans, Louisiana. J Med Entomol. 1992 Sep;29(5):802–805. doi: 10.1093/jmedent/29.5.802. [DOI] [PubMed] [Google Scholar]
  123. Turell M. J., Beaman J. R., Neely G. W. Experimental transmission of eastern equine encephalitis virus by strains of Aedes albopictus and A. taeniorhynchus (Diptera: Culicidae). J Med Entomol. 1994 Mar;31(2):287–290. doi: 10.1093/jmedent/31.2.287. [DOI] [PubMed] [Google Scholar]
  124. Turell M. J., Beaman J. R., Tammariello R. F. Susceptibility of selected strains of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) to chikungunya virus. J Med Entomol. 1992 Jan;29(1):49–53. doi: 10.1093/jmedent/29.1.49. [DOI] [PubMed] [Google Scholar]
  125. Turell M. J., Gargan T. P., 2nd, Bailey C. L. Culex pipiens (Diptera: Culicidae) morbidity and mortality associated with Rift Valley fever virus infection. J Med Entomol. 1985 May 24;22(3):332–337. doi: 10.1093/jmedent/22.3.332. [DOI] [PubMed] [Google Scholar]
  126. Vernick K. D., Collins F. H. Association of a Plasmodium-refractory phenotype with an esterase locus in Anopheles gambiae. Am J Trop Med Hyg. 1989 Jun;40(6):593–597. doi: 10.4269/ajtmh.1989.40.593. [DOI] [PubMed] [Google Scholar]
  127. Vernick K. D., Collins F. H., Gwadz R. W. A general system of resistance to malaria infection in Anopheles gambiae controlled by two main genetic loci. Am J Trop Med Hyg. 1989 Jun;40(6):585–592. doi: 10.4269/ajtmh.1989.40.585. [DOI] [PubMed] [Google Scholar]
  128. Wallis G. P., Tabachnick W. J. Genetic analysis of rock hole and domestic Aedes aegypti on the Caribbean island of Anguilla. J Am Mosq Control Assoc. 1990 Dec;6(4):625–630. [PubMed] [Google Scholar]
  129. Wallis G. P., Tabachnick W. J., Powell J. R. Genetic heterogeneity among Caribbean populations of Aedes aegypti. Am J Trop Med Hyg. 1984 May;33(3):492–498. doi: 10.4269/ajtmh.1984.33.492. [DOI] [PubMed] [Google Scholar]
  130. Wallis G. P., Tabachnick W. J., Powell J. R. Macrogeographic genetic variation in a human commensal: Aedes aegypti, the yellow fever mosquito. Genet Res. 1983 Jun;41(3):241–258. doi: 10.1017/s0016672300021315. [DOI] [PubMed] [Google Scholar]
  131. Ward R. D., Bettini S., Maroli M., McGarry J. W., Draper A. Phosphoglucomutase polymorphism in Phlebotomus perfiliewi perfiliewi Parrot (Diptera: Psychodidae) from central and northern Italy. Ann Trop Med Parasitol. 1981 Dec;75(6):653–661. doi: 10.1080/00034983.1981.11687497. [DOI] [PubMed] [Google Scholar]
  132. Warren M., Collins W. E., Richardson B. B., Skinner J. C. Morphologic variants of Anopheles albimanus and susceptibility to Plasmodium vivax and P. falciparum. Am J Trop Med Hyg. 1977 Jul;26(4):607–611. doi: 10.4269/ajtmh.1977.26.607. [DOI] [PubMed] [Google Scholar]
  133. Wattam A. R., Christensen B. M. Further evidence that the genes controlling susceptibility of Aedes aegypti to filarial parasites function independently. J Parasitol. 1992 Dec;78(6):1092–1095. [PubMed] [Google Scholar]
  134. Wattam A. R., Christensen B. M. Induced polypeptides associated with filarial worm refractoriness in Aedes aegypti. Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6502–6505. doi: 10.1073/pnas.89.14.6502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  135. Weaver S. C., Lorenz L. H., Scott T. W. Pathologic changes in the midgut of Culex tarsalis following infection with Western equine encephalomyelitis virus. Am J Trop Med Hyg. 1992 Nov;47(5):691–701. doi: 10.4269/ajtmh.1992.47.691. [DOI] [PubMed] [Google Scholar]
  136. Weaver S. C., Scott T. W., Lorenz L. H., Lerdthusnee K., Romoser W. S. Togavirus-associated pathologic changes in the midgut of a natural mosquito vector. J Virol. 1988 Jun;62(6):2083–2090. doi: 10.1128/jvi.62.6.2083-2090.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Wekesa J. W., Copeland R. S., Mwangi R. W. Effect of Plasmodium falciparum on blood feeding behavior of naturally infected Anopheles mosquitoes in western Kenya. Am J Trop Med Hyg. 1992 Oct;47(4):484–488. doi: 10.4269/ajtmh.1992.47.484. [DOI] [PubMed] [Google Scholar]
  138. Welburn S. C., Maudlin I., Ellis D. S. Rate of trypanosome killing by lectins in midguts of different species and strains of Glossina. Med Vet Entomol. 1989 Jan;3(1):77–82. doi: 10.1111/j.1365-2915.1989.tb00477.x. [DOI] [PubMed] [Google Scholar]
  139. Welburn S. C., Maudlin I. Haemolymph lectin and the maturation of trypanosome infections in tsetse. Med Vet Entomol. 1990 Jan;4(1):43–48. doi: 10.1111/j.1365-2915.1990.tb00258.x. [DOI] [PubMed] [Google Scholar]
  140. Welburn S. C., Maudlin I. Lectin signalling of maturation of T. congolense infections in tsetse. Med Vet Entomol. 1989 Apr;3(2):141–145. doi: 10.1111/j.1365-2915.1989.tb00489.x. [DOI] [PubMed] [Google Scholar]
  141. Wood R. J., Ouda N. A. The genetic basis of resistance and sensitivity to the meiotic drive gene D in the mosquito Aedes aegypti L. Genetica. 1987 May 15;72(1):69–79. doi: 10.1007/BF00126980. [DOI] [PubMed] [Google Scholar]
  142. Wu W. K., Tesh R. B. Genetic factors controlling susceptibility to Leishmania major infection in the sand fly Phlebotomus papatasi (Diptera: Psychodidae). Am J Trop Med Hyg. 1990 Apr;42(4):329–334. doi: 10.4269/ajtmh.1990.42.329. [DOI] [PubMed] [Google Scholar]
  143. Wu W. K., Tesh R. B. Selection of Phlebotomus papatasi (Diptera: Psychodidae) lines susceptible and refractory to Leishmania major infection. Am J Trop Med Hyg. 1990 Apr;42(4):320–328. doi: 10.4269/ajtmh.1990.42.320. [DOI] [PubMed] [Google Scholar]
  144. Zielke E., Kuhlow F. On the inheritance of susceptibility for infection with Wuchereria bancrofti in Culex pipiens fatigans. Tropenmed Parasitol. 1977 Mar;28(1):68–70. [PubMed] [Google Scholar]
  145. Zielke E. Untersuchungen zur Vererbung der Empfänglichkeit gegenüber der Hundefilar ie Dirofilaria immitis bei Culex pipiens fatigans und Aedes aegypti. Z Tropenmed Parasitol. 1973 Mar;24(1):36–44. [PubMed] [Google Scholar]
  146. van Driel J. W., Sluiters J. F., van der Kaay H. J. Allozyme variation in Anopheles stephensi Liston from Pakistan (Diptera: Culicidae). Biochem Genet. 1987 Dec;25(11-12):789–802. doi: 10.1007/BF00502599. [DOI] [PubMed] [Google Scholar]
  147. van der Kaay H. J., Laarman J. J., Curtis C. F., Boorsma E. G., van Seventer H. A. Susceptibility of Plasmodium berghei in a laboratory population of Anopheles atroparvus (Diptera: Culicidae) after the introduction of Plasmodium-refractory genotypes. J Med Entomol. 1982 Oct 14;19(5):536–540. doi: 10.1093/jmedent/19.5.536. [DOI] [PubMed] [Google Scholar]

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