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Conspecific Sharing of Breeding Sites by Anopheline Female Mosquitoes (Diptera: Culicidae) Inferred from Microsatellite Markers

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Abstract

The number of Anopheles gambiae and Anopheles arabiensis females that used each of the 33 sampled breeding sites in west Kenya was estimated by microsatellite markers and related statistics to test the hypothesis that conspecific females share aquatic sites. Totally, 166 An. gambiae and 168 An. arabiensis larvae were identified and were genotyped. The mean number of larvae per breeding site was 8.3 for An. gambiae and 8.4 for An. arabiensis. The likelihood method estimated that, for An. gambiae, the mean number of females that would have laid eggs per breeding site was 5.2 and ranged from 2 to 9, and for An. arabiensis, the mean was 5.0 with a range of 2–10. The clustering method estimated that the mean number of females laying eggs per breeding site was 6.8 for An. gambiae. The results provide molecular evidence that females of one or both species share breeding sites.

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References

  • 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

    Article  CAS  Google Scholar 

  • Apostol BL, Black WC IV, Reiter P, Miller BR (1994) Use of ramdomly 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 51:89–97

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chen H, Fillnger U, Yan G (2006a) Oviposition behavior of female Anopheles gambiae in western Kenya inferred from microsatellite markers. Am J Trop Med Hyg 75:246–250

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Coetzee M, Craig M, Le Sueur D (2000) Distribution of African malaria mosquitoes belonging to the Anopheles gambiae complex. Parasitol Today 16:74–77

    Article  PubMed  CAS  Google Scholar 

  • Colton YM, Chadee DD, Severson DW (2003) Natural skip oviposition of the mosquito Aedes aegypti indicated by codominant genetic markers. Med Vet Entomol 17:195–204

    Article  PubMed  CAS  Google Scholar 

  • Donnelly MJ, Townson H (2000) Evidence for extensive genetic differentiation among populations of the malaria vector, Anopheles arabiensis in East Africa. Insect Mol Biol 9:357–367

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Goodnight KF (2001) Kinship 1.2 Manual. Dept. of Ecol. and Evolutionary Biol., Rice University, Houston, TX

  • Gwadz R, Collins FH (1996) Anopheline mosquitoes and the agents they transmit. In: Beaty BJ, Marquardt WC (eds) The biology of disease vectors. University Press of Colorado, Colorado, pp 73–84

    Google Scholar 

  • Harrington LC, Edman JD (2001) Indirect evidence against delayed “skip-oviposition” behavior by Aedes aegypti (Diptera: Culicidae) in Thailand. J Med Entomol 38:641–645

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Huang J, Miller JR, Chen S, Vulule JM, Walker ED (2006) Anopheles gambiae (Diptera: Culicidae) oviposition in response to agarose media and cultured bacterial volatiles. J Med Entomol 43:498–504

    Article  PubMed  Google Scholar 

  • Kamau L, Hawley WA, Lehmann T, Orago AS, Cornel A, Ke Z, Collins FH (1998) Use of short tandem repeats for the analysis of genetic variability in sympatric populations of Anopheles gambiae and Anopheles arabiensis. Heredity 80:675–682

    Article  PubMed  CAS  Google Scholar 

  • Kamau L, Mukabana WR, Hawley WA, Lehmann T, Irungu LW, Orago AA, Collins FH (1999) Analysis of genetic variability in Anopheles arabiensis and Anopheles gambiae using microsatellite loci. Insect Mol Biol 8:287–297

    Article  PubMed  CAS  Google Scholar 

  • Lehmann T, Hawley WA, Kama 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 77:192–208

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lindsay SW, Parson L, Thomas CJ (1998) Mapping the ranges and relative abundance of the two principal African malaria vectors, Anopheles gambiae sensu stricto and An. arabiensis, using climate data. Proc R Soc Lond Series B 265:847–854

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

  • Minakawa N, Githure JI, Beier JC, Yan G (2001) Anopheline mosquito survival strategies during the dry period in western Kenya. J Med Entomol 38:388–392

    PubMed  CAS  Google Scholar 

  • Minitab (1996) Minitab Reference Manual, Version 12.2. Minitab, Pennsylvania

  • Nyanjom SRG, Chen H, Gebra-Micheal T, Bekele E, Shililu J, Githure J, Beier JC, Yan G (2003) Population genetic structure of Anopheles arabiensis mosquitoes in Ethiopia and Eritrea. J Heredity 94:457–463

    Article  CAS  Google Scholar 

  • Pates H, Curtis C (2005) Mosquito behavior and vector control. Ann Rev Entomol 50:53–70

    Article  CAS  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Rohlf FJ (2000) NTSYSpc User Guide, Version 2.1. Applied Biostatistics Inc., New York

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

  • Simard F, Fontenille D, Lehmann T, Girod R, Brutus L, Gopaul R, Dournon C, Collins FH (1999) High amounts of genetic differentiation between populations of the malaria vector Anopheles arabiensis from West Africa and Eastern outer islands. Am J Trop Med Hyg 60:1000–1009

    PubMed  CAS  Google Scholar 

  • Taylor CE, Toure YT, Coluzzi M, Petrarca V (1993) Effective population size and persistence of Anopheles arabiensis during the dry season in West Africa. Med Vet Entomol 7:351–357

    PubMed  CAS  Google Scholar 

  • Tripet F, Toure YT, Taylor CE, Norris DE, Dolo G, Lanzaro GC (2001) DNA analysis of transferred sperm reveals significant levels of gene flow between molecular forms of Anopheles gambiae. Mol Ecol 10:1725–1732

    Article  PubMed  CAS  Google Scholar 

  • Vaughan JA, Noden BH, Beier JC (1994) Sporogonic development of Plasmodium falciparum in six species of laboratory-infected Anopheles mosquitoes. Am J Trop Med Hyg 51:233–243

    PubMed  CAS  Google Scholar 

  • Wagbatsoma VA, Ogbeide O (1995) Towards malaria control in Nigeria: a qualitative study on the population of mosquitoes. J R Soc Health 115:363–365

    Article  PubMed  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. D. Amenya and two anonymous reviewers for their valuable comments on the manuscript. This research was supported by Sumitomo Foundation, UNDP/WORLD BANK/WHO Special Programme for Research and Training in Tropical Diseases (TDR), and NIH grants D43 TW01505, U19 AI45511 and R01 AI50243.

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Authors and Affiliations

  1. Program in Public Health, College of Health Sciences, University of California, Irvine, CA, 92697, USA

    Hong Chen & Guiyun Yan

  2. Nairobi Research Station, Institute of Tropical Medicine, Nagasaki University, Nairobi, Kenya

    Noboru Minakawa

  3. Department of Entomology, Pennsylvania State University, University Park, PA, 16802, USA

    Liwang Cui

  4. 3501 Hewitt Hall, Irvine, CA, 92697, USA

    Hong Chen

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  1. Hong Chen
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  2. Noboru Minakawa
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  3. Liwang Cui
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  4. Guiyun Yan
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Correspondence to Hong Chen.

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Chen, H., Minakawa, N., Cui, L. et al. Conspecific Sharing of Breeding Sites by Anopheline Female Mosquitoes (Diptera: Culicidae) Inferred from Microsatellite Markers. J Insect Behav 21, 24–33 (2008). https://doi.org/10.1007/s10905-007-9101-4

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  • DOI: https://doi.org/10.1007/s10905-007-9101-4

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