• 1.

    Alphey L, Benedict MQ, Bellini R, Clark GG, Dame DA, Service MW, Dobson SL, 2010. Sterile-insect methods for control of mosquito-borne diseases: an analysis. Vector Borne Zoonotic Dis 10: 18.

    • Search Google Scholar
    • Export Citation
  • 2.

    Carvalho DO, Nimmo D, Naish N, McKemey AR, Gray P, Wilke AB, Marrelli MT, Virginio JF, Alphey L, Capurro ML, 2014. Mass production of genetically modified Aedes aegypti for field releases in Brazil. J Vis Exp 83: 3579.

    • Search Google Scholar
    • Export Citation
  • 3.

    Harris AF, Nimmo D, McKemey AR, Kelly N, Scaife S, Donnelly CA, Beech C, Petrie WD, Alphey L, 2011. Field performance of engineered male mosquitoes. Nat Biotechnol 29: 10341037.

    • Search Google Scholar
    • Export Citation
  • 4.

    Arnqvist G, Nilsson T, 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60: 145164.

  • 5.

    Yuval B, 2006. Mating systems of blood-feeding flies. Annu Rev Entomol 51: 413440.

  • 6.

    Downe AER, 1975. Internal regulation of rate of digestion of blood meals in the mosquito, Aedes aegypti. J Insect Physiol 21: 5.

  • 7.

    Ramalingam S, Craig GB Jr, 1976. Functions of the male accessory gland secretions of Aedes mosquitoes (Diptera: Culicidae): transplantation studies. Can Entomol 108: 6.

    • Search Google Scholar
    • Export Citation
  • 8.

    Gwadz RW, Craig GB Jr, Hickey WA, 1971. Female sexual behavior as the mechanism rendering Aedes aegypti refractory to insemination. Biol Bull 140: 201214.

    • Search Google Scholar
    • Export Citation
  • 9.

    Craig GB Jr, 1967. Mosquitoes: female monogamy induced by male accessory gland substance. Science 156: 14991501.

  • 10.

    Sirot LK, Poulson RL, McKenna MC, Girnary H, Wolfner MF, Harrington LC, 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem Mol Biol 38: 176189.

    • Search Google Scholar
    • Export Citation
  • 11.

    Fuchs MS, Hiss EA, 1970. The partial purification and separation of the protein components of matrone from Aedes aegypti. J Insect Physiol 16: 931939.

    • Search Google Scholar
    • Export Citation
  • 12.

    Fuchs MS, Craig GB Jr, Hiss EA, 1968. The biochemical basis of female monogamy in mosquitoes. I. Extraction of the active principle from Aedes aegypti. Life Sci 7: 835839.

    • Search Google Scholar
    • Export Citation
  • 13.

    Sirot LK, Hardstone MC, Helinski ME, Ribeiro JM, Kimura M, Deewatthanawong P, Wolfner MF, Harrington LC, 2011. Towards a semen proteome of the dengue vector mosquito: protein identification and potential functions. PLoS Negl Trop Dis 5: e989.

    • Search Google Scholar
    • Export Citation
  • 14.

    Boes KE, Ribeiro JM, Wong A, Harrington LC, Wolfner MF, Sirot LK, 2014. Identification and characterization of seminal fluid proteins in the Asian tiger mosquito, Aedes albopictus. PLoS Negl Trop Dis 8: e2946.

    • Search Google Scholar
    • Export Citation
  • 15.

    Shutt B, Stables L, Aboagye-Antwi F, Moran J, Tripet F, 2010. Male accessory gland proteins induce female monogamy in anopheline mosquitoes. Med Vet Entomol 24: 9194.

    • Search Google Scholar
    • Export Citation
  • 16.

    Oliva CF, Damiens D, Vreysen MJ, Lemperiere G, Gilles J, 2013. Reproductive strategies of Aedes albopictus (Diptera: Culicidae) and implications for the sterile insect technique. PLoS ONE 8: e78884.

    • Search Google Scholar
    • Export Citation
  • 17.

    Spielman A, Leahy MG, Skaff V, 1967. Seminal loss in repeatedly mated female Aedes aegypti. Biol Bull 132: 8.

  • 18.

    Yuval B, Fritz GN, 1994. Multiple mating in female mosquitoes—evidence from a field population of Anopheles freeborni (Diptera: Culicidae). Bull Entomol Res 84: 4.

    • Search Google Scholar
    • Export Citation
  • 19.

    Tripet F, Toure YT, Dolo G, Lanzaro GC, 2003. Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg 68: 15.

    • Search Google Scholar
    • Export Citation
  • 20.

    Boyer S, Toty C, Jacquet M, Lemperiere G, Fontenille D, 2012. Evidence of multiple inseminations in the field in Aedes albopictus. PLoS ONE 7: e42040.

    • Search Google Scholar
    • Export Citation
  • 21.

    Helinski ME, Valerio L, Facchinelli L, Scott TW, Ramsey J, Harrington LC, 2012. Evidence of polyandry for Aedes aegypti in semifield enclosures. Am J Trop Med Hyg 86: 635641.

    • Search Google Scholar
    • Export Citation
  • 22.

    Darsie RJ, Ward R, 2005. Identification and Geographical Distribution of the Mosquitoes of North America, North of Mexico. Gainesville, FL: University Press of Florida.

    • Search Google Scholar
    • Export Citation
  • 23.

    Brown JE, McBride CS, Johnson P, Ritchie S, Paupy C, Bossin H, Lutomiah J, Fernandez-Salas I, Ponlawat A, Cornel AJ, Black WC, Gorrochotegui-scalante N, Urdaneta-Marquez L, Sylla M, Slotman M, Murray KO, Walker C, Powell JR, 2011. Worldwide patterns of genetic differentiation imply multiple ‘domestications’ of Aedes aegypti, a major vector of human diseases. Proc Biol Sci 278: 24462454.

    • Search Google Scholar
    • Export Citation
  • 24.

    R Core Team, 2013. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at: http://www.R-project.org/.

    • Search Google Scholar
    • Export Citation
  • 25.

    Rousset F, 2008. genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103106.

  • 26.

    Guo SW, Thompson EA, 1992. Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48: 361372.

  • 27.

    Rice WR, 1989. Analyzing tables of statistical tests. Evolution 43: 223225.

  • 28.

    Jones AG, 2005. gerud 2.0: a computer program for the reconstruction of parental genotypes from half-sib progeny arrays with known or unknown parents. Mol Ecol Notes 5: 708711.

    • Search Google Scholar
    • Export Citation
  • 29.

    Jones AG, Ardren WR, 2003. Methods of parentage analysis in natural populations. Mol Ecol 12: 25112523.

  • 30.

    Dodds KG, Tate ML, McEwan JC, Crawford AM, 1996. Exclusion probabilities for pedigree testing farm animals. Theor Appl Genet 92: 9.

  • 31.

    Slotman MA, Kelly NB, Harrington LC, Kitthawee S, Jones JW, Scott TW, Caccone A, Powell JR, 2006. Polymorphic microsatellite markers for studies of Aedes aegypti (Diptera: Culicidae), the vector of dengue and yellow fever. Mol Ecol Notes 7: 168171.

    • Search Google Scholar
    • Export Citation
  • 32.

    Gillies MT, 1956. A new character for the recognition of nulliparous females of Anopheles gambiae. Bull World Health Organ 15: 451459.

  • 33.

    Fansiri T, Fontaine A, Diancourt L, Caro V, Thaisomboonsuk B, Richardson JH, Jarman RG, Ponlawat A, Lambrechts L, 2013. Genetic mapping of specific interactions between Aedes aegypti mosquitoes and dengue viruses. PLoS Genet 9: e1003621.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Evidence of Limited Polyandry in a Natural Population of Aedes aegypti

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  • Department of Ecology and Evolution, Yale University, New Haven, Connecticut; School of Public Health and Tropical Medicine, Tulane University, New Orleans, Louisiana
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The mosquito Aedes aegypti is a vector of yellow fever, dengue, and chikungunya. Control of the insect is crucial to stop the spread of dengue and chikungunya, so it is critically important to understand its mating behavior. Primarily, based on laboratory behavior, it has long been assumed that Ae. aegypti females mate once in their lifetime. However, multiple inseminations have been observed in semi-field and laboratory settings, and in closely related species. Here, we report the first evidence of polyandry in a natural population of Ae. aegypti. Female Ae. aegypti were captured around the New Orleans, LA, metropolitan area. They were offered a blood meal and allowed to lay eggs, which were reared to the third-instar larval stage. A parentage analysis using four microsatellite loci was performed. Out of 48 families, 3 showed evidence of multiple paternity. An expanded analysis of these three families found that one family group included offspring contributed by three fathers, and the other two included offspring from two fathers. This result establishes that polyandry can occur in a small proportion of Ae. aegypti females in a natural setting. This could complicate future genetic control efforts and has implications for sampling for population genetics.

Author Notes

* Address correspondence to Joshua B. Richardson, Department of Ecology and Evolutionary Biology, Yale University, 21 Sachem Street, ESC, rm 158B, New Haven, CT 06520. E-mail: joshua.richardson@yale.edu

Authors' addresses: Joshua B. Richardson, Andrea Gloria-Soria, and Jeffrey Powell, Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, E-mails: joshua.richardson@yale.edu, andrea.gloria-soria@yale.edu, and jeffrey.powell@yale.edu. Samuel B. Jameson and Dawn Wesson, Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, LA, E-mails: sbishop@tulane.edu and wesson@tulane.edu.

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