Competitive Reduction by Satyrization? Evidence for Interspecific Mating in Nature and Asymmetric Reproductive Competition between Invasive Mosquito Vectors

Frederic Tripet Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by Frederic Tripet in
Current site
Google Scholar
PubMed
Close
,
L. Philip Lounibos Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by L. Philip Lounibos in
Current site
Google Scholar
PubMed
Close
,
Dannielle Robbins Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by Dannielle Robbins in
Current site
Google Scholar
PubMed
Close
,
Jenny Moran Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by Jenny Moran in
Current site
Google Scholar
PubMed
Close
,
Naoya Nishimura Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by Naoya Nishimura in
Current site
Google Scholar
PubMed
Close
, and
Erik M. Blosser Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, United Kingdom; Florida Medical Entomology Laboratory, University of Florida, Vero Beach, Florida

Search for other papers by Erik M. Blosser in
Current site
Google Scholar
PubMed
Close
Restricted access

Upon mating, male mosquitoes transfer accessory gland proteins (Acps) that induce refractoriness to further mating in females. This can also occur because of cross-insemination by males of related species, a process known as mating interference (satyrization). This mechanism could explain the competitive displacement of resident Aedes aegypti by the invasive Aedes albopictus where they co-occur. We tested this hypothesis in mosquito populations in Florida. A new polymerase chain reaction species diagnostic applied to sperm dissected from 304 field-collected females revealed bidirectional cross-mating in five (1.6%) individuals. Cross-injections of females with Acps showed that Ae. albopictus males induced monogamy in heterospecific females but not Ae. aegypti males. Despite its low frequency in the areas under study, the first evidence of cross-mating in nature and the asymmetric effect of Acps on mating suggest that satyrization may have initially contributed to the observed competitive reduction of Ae. aegypti by invasive Ae. albopictus in many areas.

Author Notes

*Address correspondence to Frederic Tripet, Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK. E-mail: f.tripet@biol.keele.ac.uk

Financial support: This research was supported by QR funding to FT from Keele University and a NIH grant 2R01 AI044973 to LPL.

Authors' addresses: Frederic Tripet, Dannielle Robbins, and Jenny Moran, Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Keele, Staffordshire, UK, E-mails: f.tripet@biol.keele.ac.uk, dannii_robbins@hotmail.com, and moranjenny@aol.com. L. Philip Lounibos, Naoya Nishimura, and Erik M. Blosser, Florida Medical Entomology Laboratory, University of Florida, Vero Beach, FL, E-mails: lounibos@ufl.edu, nishimur@ufl.edu, and eblosser@ufl.edu.

Reprint requests: Frederic Tripet, Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK, E-mail: f.tripet@biol.keele.ac.uk.

  • 1.

    Gröning J, Hochkirch A, 2008. Reproductive interference between animal species. Q Rev Biol 83: 257282.

  • 2.

    Ribeiro JM, 1988. Can satyrs control pests and vectors? J Med Entomol 25: 431440.

  • 3.

    Ribeiro JM, Spielman A, 1986. The satyr effect: a model predicting parapatry and species extinction. Am Nat 128: 513528.

  • 4.

    Lounibos LP, 2007. Competitive displacement and reduction. Floore TG, ed. Biorational Control of Mosquitoes. Am Mosq Control Assoc Bull No. 7, 276282.

    • Search Google Scholar
    • Export Citation
  • 5.

    Huang Y-M, 1972. Contributions to the mosquito fauna of Southeast Asia. XIV. The subgenus Stegomyia of Aedes in Southeast Asia. 1. The scutellaris group of species (Diptera: Culicidae). Contrib Am Entomol Inst 9: 1109.

    • Search Google Scholar
    • Export Citation
  • 6.

    Huang Y-M, 2004. The subgenus Stegomyia of Aedes of the Afrotropical Region with keys to the species (Diptera: Culicidae). Zootaxa 700: 1120.

    • Search Google Scholar
    • Export Citation
  • 7.

    Lounibos LP, 2002. Invasions by insect vectors of human disease. Annu Rev Entomol 47: 233266.

  • 8.

    Paupy C, Ollomo B, Kamgang B, Moutailler S, Rousset D, Demanou M, Hervé JP, Leroy E, Simard F, 2010. Comparative role of Aedes albopictus and Aedes aegypti in the emergence of dengue and chikungunya in Central Africa. Vector Borne Zoonotic Dis 10: 259267.

    • Search Google Scholar
    • Export Citation
  • 9.

    Hartberg WK, 1970. Observations on the mating behavior of Aedes aegypti in nature. Bull World Health Organ 45: 847850.

  • 10.

    Gubler DJ, Bhattacharya NC, 1972. Swarming and mating of Aedes (S.) albopictus in nature. Mosq News 32: 219223.

  • 11.

    Leahy MG, Craig GB, 1967. Barriers to hybridization between Aedes aegypti and Aedes albopictus. Evolution 21: 4158.

  • 12.

    Nijhout HF, Craig GB, 1971. Reproductive isolation in Stegomyia mosquitoes. III Evidence for a sexual pheromone. Entomol Exp Appl 14: 399412.

    • Search Google Scholar
    • Export Citation
  • 13.

    Brogdon WG, 1994. Measurement of flight tone differences between female Aedes aegypti and A. albopictus (Diptera: Culicidae). J Med Entomol 31: 700703.

    • Search Google Scholar
    • Export Citation
  • 14.

    Harper JP, Paulson SL, 1994. Reproductive isolation between Florida strains of Aedes aegypti and Aedes albopictus. J Am Mosq Control Assoc 10: 8892.

    • Search Google Scholar
    • Export Citation
  • 15.

    Nasci RS, Hare CG, Willis FS, 1989. Interspecific mating between Louisiana strains of Aedes albopictus and Aedes aegypti in the field and the laboratory. J Am Mosq Control Assoc 5: 15.

    • Search Google Scholar
    • Export Citation
  • 16.

    Craig GB, 1993. The diaspora of the Asian Tiger Mosquito. McKnight BN, ed. Biological Pollution: The Control and Impact of Invasive Exotic Species. Indianapolis, IN: Indiana Academy of Sciences, 101120.

    • Search Google Scholar
    • Export Citation
  • 17.

    Klowden MJ, 1999. The check is in the male: male mosquitoes affect female physiology and behavior. J Am Mosq Control Assoc 15: 213220.

    • Search Google Scholar
    • Export Citation
  • 18.

    De Buck A, 1942. Kreuzungsversuche mit Stegomyia fasciatus Fabricius and S. albopicta Skuse. Zeitsch Angew Entomol 19: 309312.

  • 19.

    Leahy MG, Craig GB, 1965. Accessory gland substance as a stimulant for oviposition in Aedes aegypti and Ae. albopictus. Mosq News 21: 448452.

    • Search Google Scholar
    • Export Citation
  • 20.

    Lounibos LP, O'Meara GF, Juliano SA, Nishimura N, Escher RL, Reiskind MH, Cutwa M, Greene K, 2010. Differential survivorship of invasive mosquito species in south Florida cemeteries: do site-specific microclimates explain patterns of coexistence and exclusion? Ann Entomol Soc Am 103: 757770.

    • Search Google Scholar
    • Export Citation
  • 21.

    Tripet F, Touré Y, Taylor CE, Norris DE, Dolo G, Lanzaro GC, 2001. DNA analysis of transfered sperm reveals significant levels of gene flow between molecular forms of the Anopheles gambiae complex. Mol Ecol 10: 17251732.

    • Search Google Scholar
    • Export Citation
  • 22.

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

    • Search Google Scholar
    • Export Citation
  • 23.

    Tripet F, Thielman T, Lanzaro GC, 2005. The effect of seminal fluids on mating between the Anopheles gambiae M and S forms. J Med Entomol 42: 596603.

    • Search Google Scholar
    • Export Citation
  • 24.

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

  • 25.

    Wu CC, Fallon AM, 1998. Analysis of a ribosomal DNA intergenic spacer region from the yellow fever mosquito, Aedes aegypti. Insect Mol Biol 7: 1929.

    • Search Google Scholar
    • Export Citation
  • 26.

    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
  • 27.

    Hayes RO, 1953. Determination of a physiological saline solution for Aedes aegypti (L.). J Econ Entomol 10: 8892.

  • 28.

    SAS Institute Inc., 2007. JMP Statistics and Graphics Guide. Cary, NC.

  • 29.

    O'Meara GF, Gettman AD, Evans LF, Curtis GA, 1993. The spread of Aedes albopictus in Florida. Am Entomol 39: 163172.

  • 30.

    O'Meara GF, Evans LF, Gettman AD, Cuda JP, 1995. Spread of Aedes albopictus and decline of Ae. aegypti (Diptera: Culicidae) in Florida. J Med Entomol 32: 554562.

    • Search Google Scholar
    • Export Citation
  • 31.

    Juliano SA, 1998. Species introduction and replacement among mosquitoes: interspecific resource competition or apparent competition? Ecology 79: 255268.

    • Search Google Scholar
    • Export Citation
  • 32.

    Juliano SA, Lounibos LP, 2005. Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8: 558574.

  • 33.

    Hobbes JH, Hughes EA, Eichold BH, 1991. Replacement of Aedes aegypti by Aedes albopictus in Mobile, Alabama. J Am Mosq Control Assoc 7: 488489.

    • Search Google Scholar
    • Export Citation
  • 34.

    Kaplan L, Kendell D, Robertson D, Livdahl T, Katchikian C, 2010. Aedes aegypti and Aedes albopictus in Bermuda: extinction, invasion, invasion and extinction. Biol Invas 12: 32773288.

    • Search Google Scholar
    • Export Citation
  • 35.

    Braks MA, Honório NA, Lounibos LP, Lourenco-De-Oliveira R, Juliano SA, 2004. Interspecific competition between two invasive species of container mosquitoes, Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in Brazil. Ann Entomol Soc Am 97: 130139.

    • Search Google Scholar
    • Export Citation
  • 36.

    Bagny L, DeLatte H, Elissa N, Quilici S, Fontenille D, 2009. Aedes (Diptera: Culicidae) vectors of arboviruses in Mayotte (Indian Ocean): distribution area and larval habitats. J Med Entomol 46: 198207.

    • Search Google Scholar
    • Export Citation
  • 37.

    Braks MA, Honório NA, Lourenço-de-Oliveira R, Juliano SA, Lounibos LP, 2003. Convergent habitat segregation of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) in southeastern Brazil and Florida, USA. J Med Entomol 40: 785794.

    • Search Google Scholar
    • Export Citation
  • 38.

    Gubler DJ, 1970. Induced sterility in Aedes (Stegomyia) polynesiensis marks by cross-inseminating with Aedes (Stegomyia) albopictus Skuse. J Med Entomol 7: 6570.

    • Search Google Scholar
    • Export Citation
  • 39.

    Rozeboom LE, Bridges JR, 1972. Relative population densities of Aedes albopictus and A. guamensis on Guam. Bull World Health Organ 46: 477483.

    • Search Google Scholar
    • Export Citation
  • 40.

    Jones JC, 1968. The sexual life of a mosquito. Sci Am 218: 108116.

  • 41.

    Spielman A, Leahy MG, Skaff V, 1967. Seminal loss in repeatedly mated female Aedes aegypti. Biol Bull 132: 404412.

  • 42.

    Young AD, Downe AE, 1982. Renewal of sexual receptivity in mated female mosquitoes, Aedes aegypti. Physiol Entomol 7: 467471.

  • 43.

    Spielman A, 1964. The mechanics of copulation in Aedes aegypti. Biol Bull 127: 324344.

  • 44.

    Sirot LK, Poulson RL, Caitlin McKenna M, 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
  • 45.

    Rogers DW, Whitten MM, Thailayil J, Soichot J, Levashina EA, Catteruccia F, 2008. Molecular and cellular components of the mating machinery in Anopheles gambiae females. Proc Natl Acad Sci USA 105: 1939019395.

    • Search Google Scholar
    • Export Citation
  • 46.

    Pondeville E, Maria A, Jacques JC, Bourgouin C, Dauphin-Villemant C, 2008. Anopheles gambiae males produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating. Proc Natl Acad Sci USA 105: 1963119636.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 42 42 21
Full Text Views 617 160 3
PDF Downloads 196 46 3
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save