OVIPOSITION BEHAVIOR OF FEMALE ANOPHELES GAMBIAE IN WESTERN KENYA INFERRED FROM MICROSATELLITE MARKERS

HONG CHEN Program in Public Health, College of Health Sciences, University of California, Irvine, California; Mbita Point Research and Training Center, International Center of Insect Physiology and Ecology, Nyanza Province, Kenya

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ULRIKE FILLINGER Program in Public Health, College of Health Sciences, University of California, Irvine, California; Mbita Point Research and Training Center, International Center of Insect Physiology and Ecology, Nyanza Province, Kenya

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GUIYUN YAN Program in Public Health, College of Health Sciences, University of California, Irvine, California; Mbita Point Research and Training Center, International Center of Insect Physiology and Ecology, Nyanza Province, Kenya

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Anopheles gambiae females in a relatively isolated hut and all larvae from larval habitats within 100 m of the hut were collected in August 2001 in western Kenya. Among 42 aquatic habitats, 16 had A. gambiae larvae. Two hundred fifty larvae and 58 adults were genotyped using nine microsatellite markers to infer sibling relationship between the larvae and maternity between the females and larvae. The pairwise genetic relatedness of A. gambiae larvae per habitat ranged from −0.4112 to 0.9375, indicating that full siblings, half siblings, and genetically unrelated individuals presented at those habitats with multiple larvae. From a likelihood analysis, it was estimated that 56.6% of females had larvae in multiple habitats. These results substantiate that one A. gambiae female uses multiple breeding sites for oviposition, and thus, average genetic relatedness for breeding sites with high larval populations tends to be low.

Author Notes

Reprint requests: Hong Chen, 3501 Hewitt Hall, Program in Public Health, College of Health Sciences, University of California-Irvine, Irvine, CA 92697. E-mail: entomail@gmail.com.
  • 1

    Gillies MT, Coetzee M, 1987. A supplement to the Anophelinae of Africa south of the Sahara. South African Inst Med Res 55 :1–143.

  • 2

    Pates H, Curtis C, 2005. Mosquito behavior and vector control. Annu Rev Entomol 50 :53–70.

  • 3

    McCrae AWR, 1983. Oviposition by African malaria vector mosquitoes I. Temporal activity pattern of caged, wild-caught, freshwater Anopheles gambiae Giles sensu lato. Ann Trop Med Parasitol 77 :615–625.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    McCrae AWR, 1984. Oviposition by African malaria vector mosquitoes II. Effects of site tone, water type and conspecific immatures on target selection by freshwater Anopheles gambiae Giles sensu lato. Ann Trop Med Parasitol 78 :307–318.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Huang J, Walker ED, Giroux PY, Vulule J, Miller JR, 2005. Ovipositional site selection by Anopheles gambiae: Influences of substrate moisture and texture. Med Vet Entomol 19 :442–450.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Service MW, 1973. Identification of predators of Anopheles gambiae resting in huts, by the precipitin test. Trans R Soc Trop Med Hyg 67 :33–34.

  • 7

    Service MW, 1976. Mosquito Ecology. New York: John Wiley & Sons.

  • 8

    Minakawa N, Mutero CM, Githure JI, Beier JC, Yan G, 1999. Spatial distribution and habitat characterization of anopheline mosquito larvae in western Kenya. Am J Trop Med Hyg 61 :1010–1016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Minakawa N, Sonye G, Mogi M, Yan G, 2004. Habitat characteristics of Anopheles gambiae s.s. larvae in a Kenyan highland. Med Vet Entomol 18 :301–305.

  • 10

    Minakawa N, Sonye G, Yan G, 2005. Relationships between occurrence of Anopheles gambiae s. l. (Diptera: Culicidae) and size and stability of larval habitats. J Med Entomol 42 :295–300.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Gimnig JE, Ombok M, Kamau L, Hawley WA, 2001. Characteristics of larval anopheline (Diptera: Culicidae) habitats in western Kenya. J Med Entomol 38 :282–288.

  • 12

    Barasa SS, Hassanali A, Mbogo C, Tsanuo MK, Gachanja A, Githure J, Beier J, 2003. The use of static headspace, gas chromatography-mass spectrometry and chemometric analytical techniques in assigning chemical fingerprints to breeding sites of different mosquito species. Am J Trop Med Hyg 69 (Suppl 3):208.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Fillinger U, Knols BGJ, Becker N, 2003. Efficacy and efficiency of new Bacillus thuringiensis var. israelensis and Bacillus sphaericus formulations against Afrotropical anophelines in western Kenya. Trop Med Int Health 8 :37–47.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Kaufman MG, Oteino S, Walker ED, Vulule J, 2003. Shading and soil type influences on larval Anopheles gambiae growth under simulated natural habitat conditions. Am J Trop Med Hyg 69 (Suppl 3):453–454.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Knols BGJ, Sumba LA, Guda TO, Deng AL, Hassanali A, Beier JC, 2004. Mediation of oviposition site selection in the African malaria mosquito Anopheles gambiae (Diptera: Culicidae) by semiochemicals of microbial origin. Int J Trop Insect Sci 24 :260–265.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Sumba LA, Okoth K, Deng AL, Githure J, Knols BGJ, Beier JC, Hassanali A, 2004. Daily oviposition patterns of the African malaria mosquito Anopheles gambiae Giles (Diptera: Culicidae) on different types of aqueous substrates. J Circadian Rhythms 2 :6–7.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Munga S, Minakawa N, Zhou G, Barrack OJ, Githeko AK, Yan G, 2005. Oviposition site preference and egg hatchability of Anopheles gambiae: Effects of land cover types. J Med Entomol 42 :993–997.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Blackwell A, Johnson SN, 2000. Electrophysiological investigation of larval water and potential oviposition chemoattractants for Anopheles gambiae s. s. Ann Trop Med Parasitol 94 :389–398.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Rejmankova E, Higashi R, Roberts D, Lege M, Andre R, 2000. Detection of a potential oviposition attractant for Anopheles albimanus Wiedemann using solid-phase microextraction fibers in situ. Aquat Ecol 34 :413–420.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Rejmankova E, Higashi R, Grieco J, Achiee N, Roberts D, 2005. Volatile substances from larval habitats mediate species-specific oviposition in Anopheles mosquitoes. J Med Entomol 42 :95–103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Minakawa N, Pamela P, Yan G, 2002. Influence of host and larval habitat distribution on the abundance of African malaria vectors in western Kenya. Am J Trop Med Hyg 67 :32–38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Fay RW, Perry AS, 1965. Laboratory studies of ovipositional preferences of Aedes aegypti. Mosq News 25 :276–281.

  • 23

    Chadee DD, Corbet PS, Gresnwood JJD, 1990. Egg-laying yellow fever mosquitoes avoid sites containing eggs laid by themselves or by conspecifics. Entomol Exp Appl 57 :295–298.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Corbet PS, Chadee DD, 1993. An improved method for detecting substrate preferences shown by mosquitoes that exhibit “skip oviposition.” Phys Entomol 18 :114–118.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Chadee DD, Corbet PS, 1987. Seasonal incidence and diel patterns of oviposition in the field of the mosquito, Aedes aegypti (L.) (Diptera: Culicidae) in Trinidad, West Indies: A preliminary study. Ann Trop Med Hyg 81 :151–161.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Apostol BL, Black WC IV, Reiter P, Miller BP, 1994. Use of randomly amplified polymorphic DNA amplified by polymerase chain reaction markers to estimate the number of Aedes aegypti families at oviposition sites in San Juan, Puerto Rico. Am J Trop Med Hyg 51 :87–97.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Reiter PM, Amador A, Anderson RA, Clark GG, 1995. Short report: Dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium-marked eggs. Am J Trop Med Hyg 52 :177–179.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Wagbatsoma VA, Ogbeide O, 1995. Towards malaria control in Nigeria: A qualitative study on the population of mosquitoes. J R Soc Heal 115 :363–365.

  • 29

    Apostol BL, Black WC IV, Miller BR, Reiter P, Beaty BJ, 1993. Estimation of the number of full-sibling families at an oviposition site using RAPD-PCR markers: Applications to the mosquito Aedes aegypti. Theor Appl Genet 86 :991–1000.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zheng L, Benedict MQ, Cornel AJ, Collins FH, Kafatos FC, 1996. An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. Genetics 143 :941–952.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Blouin MS, Parsons M, Lacaille V, Lotz S, 1996. Use of microsatellite loci to classify individuals by relatedness. Mol Ecol 5 :393–401.

  • 32

    Besansky NJ, Lehmann T, Fahey GT, Fontenille D, Braack LEO, Hawley WA, Collins FH, 1997. Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow. Genetics 147 :1817–1828.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    World Health Organization, 1975. Manual on Practical Entomology in Malaria. Part II. Methods and Techniques. Geneva: World Health Organization.

    • PubMed
    • Export Citation
  • 34

    Yan G, Christensen BM, Severson DW, 1997. Comparisons of genetic variability and genome structure among mosquito strains selected for refractoriness to a malaria parasite. J Hered 88 :187–194.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Scott JA, Collins BWG, 1993. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49 :520–529.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Chen H, Githeko AK, Zhou G, Githure JI, Yan G, 2006. New records of Anopheles arabiensis breeding on the Mount Kenya highlands indicate indigenous malaria transmission. Malaria J 5 :17.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Nyanjom S, Chen H, Gebre-Michael T, Bekele E, Shililu J, Githure J, Beier J, Yan G, 2003. Population genetic structure of Anopheles arabiensis mosquitoes in Ethiopia and Eritrea. J Hered 94 :457–463.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Chen H, Minakawa N, Beier J, Yan G, 2004. Population genetic structure of Anopheles gambiae mosquitoes on Lake Victoria islands, west Kenya. Malaria J 3 :48.

  • 39

    Lehmann T, Hawley WA, Kamau L, Fontenille D, Simard F, Collins FH, 1996. Genetic differentiation of Anopheles gambiae populations from East and West Africa: comparison of microsatellite and allozyme loci. Heredity 77 :192–200.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Queller DC, Goodnight KF, 1989. Estimating relatedness using genetic markers. Evol Int J Org Evol 43 :258–275.

  • 41

    Lehmann T, Licht M, Gimnig JE, Hightower A, Vulule JM, Hawley WA, 2003. Spatial and temporal variation in kinship among Anopheles gambiae (Diptera: Culicidae) mosquitoes. J Med Entomol 40 :421–429.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    Minitab, 1996. Minitab Reference Manual, Version 12.2. State College, PA: Minitab.

    • PubMed
    • Export Citation
  • 43

    Marshall T, Slate J, Kruuk LEB, Pemberon JM, 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7 :639–655.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44

    Hall TA, 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41 :95–98.

  • 45

    Beard CB, Hamm DM, Collins FH, 1993. The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol 2 :103–124.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46

    Gwadz R, Collins FH, 1996. Anopheline mosquitoes and the agents they transmit. Beaty BJ, Marquardt WC, eds. The Biology of Disease Vectors. Boulder, CO: University Press of Colorado, 73–84.

    • PubMed
    • Export Citation
  • 47

    Killeen GK, Fillinger U, Knols BGJ, 2002. Advantages of larval control for African malaria vectors: Low mobility and behavioural responsiveness of immature mosquito stages allow high effective coverage. Malaria J 1 :8.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48

    Donnelly MJ, Licht MC, Lehmann T, 2001. Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae. Mol Bio Evol 18 :1353–1364.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49

    Schneider P, Takken W, Mccall PJ, 2000. Interspecific competition between sibling species larvae of Anopheles arabiensis and An. gambiae. Med Vet Entomol 14 :165–170.

    • PubMed
    • Search Google Scholar
    • Export Citation
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