Behavioral Ecology and Sociobiology

, Volume 66, Issue 8, pp 1131–1140 | Cite as

The role of male harassment on female fitness for the dengue vector mosquito Aedes aegypti

Original Paper

Abstract

Sexual harassment studies in insects suggest that females can incur several kinds of costs from male harassment and mating. Here, we examined direct and indirect costs of male harassment on components of female fitness in the predominantly monandrous mosquito Aedes aegypti. To disentangle the costs of harassment versus the costs of mating, we held females at a low or high density with males whose claspers were modified to prevent insemination and compared these to females held with normal males and to those held with females or alone. A reduced longevity was observed when females were held under high-density conditions with males or females, regardless if male claspers had been modified. There was no consistent effect of harassment on female fecundity. Net reproductive rate (R0) was higher in females held at low density with normal males compared to females held with males in the other treatments, even though only a small number of females showed direct evidence of remating. Indirect costs and benefits that were not due to harassment alone were observed. Daughters of females held with normal males at high density had reduced longevity compared to daughters from females held without conspecifics. However, their fitness (R0) was higher compared to females in all other treatments. Overall, our results indicate that A. aegypti females do not suffer a fitness cost from harassment of males when kept at moderate densities, and they suggest the potential for benefits obtained from ejaculate components.

Keywords

Aedes aegypti Monandry Harassment Longevity Net reproductive rate 

Supplementary material

265_2012_1365_MOESM1_ESM.doc (248 kb)
ESM 1DOC 248 kb

References

  1. Arnqvist G, Andrés JA (2006) The effects of experimentally induced polyandry on female reproduction in a monandrous mating system. Ethology 112:748–756CrossRefGoogle Scholar
  2. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164PubMedCrossRefGoogle Scholar
  3. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  4. Arnqvist G, Edvardsson M, Friberg U, Nilsson T (2000) Sexual conflict promotes speciation in insects. P Natl Acad Sci USA 97:10460–10464CrossRefGoogle Scholar
  5. Bateman PW, Ferguson JWH, Yetman CA (2006) Courtship and copulation, but not ejaculate, reduce the longevity of female field crickets (Gryllus bimaculatus). J Zool 268:341–346CrossRefGoogle Scholar
  6. Begon M, Townsend CR, Harper JL (1996) Ecology: from individuals to ecosystems. Blackwell, OxfordGoogle Scholar
  7. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300Google Scholar
  8. Bernardo J (1996) Maternal effects in animal ecology. Amer Zool 36:83–105Google Scholar
  9. Blanckenhorn WU, Hosken DJ, Martin OY, Reim C, Teuschl Y, Ward PI (2002) The costs of copulating in the dung fly Sepsis cynipsea. Behav Ecol 13:353–358CrossRefGoogle Scholar
  10. Cator LJ, Harrington LC (2011) The harmonic convergence of fathers predicts the mating success of sons in the yellow fever mosquito. Anim Behav 82:629–633CrossRefGoogle Scholar
  11. Cator LJ, Arthur BJ, Ponlawat A, Harrington LC (2011) Behavioral observations and sound recordings of free-flight mating swarms of Ae. aegypti in Thailand. J Med Entomol 48:941–946PubMedCrossRefGoogle Scholar
  12. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244PubMedCrossRefGoogle Scholar
  13. Clements AN (1999) The biology of mosquitoes. CABI, WallingfordGoogle Scholar
  14. Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365CrossRefGoogle Scholar
  15. Cox DR (1972) Regression models and life tables (with Discussion). J Roy Stat Soc B 34(2):187–220Google Scholar
  16. Craig GB (1967) Mosquitoes: female monogamy induced by male accessory gland substance. Science 156:1499–1501PubMedCrossRefGoogle Scholar
  17. Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature 407:855–856PubMedCrossRefGoogle Scholar
  18. den Hollander M, Gwynne DT (2009) Female fitness consequences of male harassment and copulation in seed beetles, Callosobruchus maculatus. Anim Behav 78:1061–1070CrossRefGoogle Scholar
  19. Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, CambridgeGoogle Scholar
  20. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  21. Eberhard WG (2004) Male–female conflict and genitalia: failure to confirm predictions in insects and spiders. Biol Rev Camb Philos Soc 79:121–186PubMedCrossRefGoogle Scholar
  22. Ferguson HM, John B, Ng’habi K, Knols BG (2005) Redressing the sex imbalance in knowledge of vector biology. Trends Ecol Evol 20:202–209PubMedCrossRefGoogle Scholar
  23. Ferguson HM, Dornhaus A, Beeche A, Borgemeister C, Gottlieb M, Mulla MS, Gimnig JE, Fish D, Killeen GF (2010) Ecology: a prerequisite for malaria elimination and eradication. PLoS Med 7:e1000303PubMedCrossRefGoogle Scholar
  24. Garcia-Rejon J, Lorono-Pino MA, Farfan-Ale JA, Flores-Flores L, Del Pilar Rosado-Paredes E, Rivero-Cardenas N, Najera-Vazquez R, Gomez-Carro S, Lira-Zumbardo V, Gonzalez-Martinez P, Lozano-Fuentes S, Elizondo-Quiroga D, Beaty BJ, Eisen L (2008) Dengue virus-infected Aedes aegypti in the home environment. Am J Trop Med Hyg 79:940–950PubMedGoogle Scholar
  25. Gay L, Eady PE, Vasudev R, Hosken DJ, Tregenza T (2009) Costly sexual harassment in a beetle. Physiol Entom 34:86–92CrossRefGoogle Scholar
  26. Grech K, Maung LA, Read AF (2007) The effect of parental rearing conditions on offspring life history in Anopheles stephensi. Malar J 6:130PubMedCrossRefGoogle Scholar
  27. Gwadz RW, Craig GB Jr, Hickey WA (1971) Female sexual behavior as the mechanism rendering Aedes aegypti refractory to insemination. Biol Bull 140:201–214PubMedCrossRefGoogle Scholar
  28. Harrington LC, Edman JD, Scott TW (2001) Why do female Aedes aegypti (Diptera: Culicidae) feed preferentially and frequently on human blood? J Med Entomol 38:411–422PubMedCrossRefGoogle Scholar
  29. Harrington LC, Scott TW, Lerdthusnee K, Coleman RC, Costero A, Clark GG, Jones JJ, Kitthawee S, Kittayapong P, Sithiprasasna R, Edman JD (2005) Dispersal of the dengue vector Aedes aegypti within and between rural communities. Am J Trop Med Hyg 72:209–220PubMedGoogle Scholar
  30. Hartberg WK (1971) Observations on the mating behaviour of Aedes aegypti in nature. Bull World Health Organ 45:847–850PubMedGoogle Scholar
  31. Helinski MEH, Harrington LC (2011) Male mating history and body size influence female fecundity and longevity of the dengue vector Aedes aegypti. J Med Entomol 48:202–211PubMedCrossRefGoogle Scholar
  32. Helinski MEH, 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 86:635–641PubMedCrossRefGoogle Scholar
  33. Howell PI, Knols BG (2009) Male mating biology. Malar J 8(Suppl 2):S8PubMedCrossRefGoogle Scholar
  34. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64PubMedCrossRefGoogle Scholar
  35. Jones TM (1974) Sexual activities during single and multiple co-habitations in Aedes aegypti mosquitoes. J Entomol 48:185–194Google Scholar
  36. Mahmood F, Reisen WK (1980) Anopheles culicifacies the occurrence of multiple insemination under laboratory conditions. Entomol Exp Appl 27:69–76CrossRefGoogle Scholar
  37. Morrow EH, Arnqvist G, Pitnick S (2003) Adaptation versus pleiotropy: why do males harm their mates? Behav Ecol 14:802–806CrossRefGoogle Scholar
  38. Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407PubMedCrossRefGoogle Scholar
  39. Muhlhauser C, Blanckenhorn WU (2002) The cost of avoiding matings in the dung fly Sepsis cynipsea. Behav Ecol 13:359–365CrossRefGoogle Scholar
  40. Parker GA (2006) Sexual conflict over mating and fertilization: an overview. Phil Trans R Soc B 361:235–259PubMedCrossRefGoogle Scholar
  41. Perich MJ, Davila G, Turner A, Garcia A, Nelson M (2000) Behavior of resting Aedes aegypti (Culicidae: Diptera) and its relation to ultra-low volume adulticide efficacy in Panama City, Panama. J Med Entomol 37:541–546PubMedCrossRefGoogle Scholar
  42. Ponlawat A, Harrington LC (2007) Age and body size influence male sperm capacity of the dengue vector Aedes aegypti (Diptera: Culicidae). J Med Entomol 44:422–426PubMedCrossRefGoogle Scholar
  43. Rodriguez-Munoz R, Bretman A, Slate J, Walling CA, Tregenza T (2010) Natural and sexual selection in a wild insect population. Science 328:1269–1272PubMedCrossRefGoogle Scholar
  44. Ronn J, Katvala M, Arnqvist G (2006) The cost of mating and egg production in Callosobruchus seed beetles. Anim Behav 72:335–342CrossRefGoogle Scholar
  45. Rossi BH, Nonacs P, Pitts-Singer TL (2010) Sexual haressment by males reduces female fecundity in the alfalfa leafcutting bee, Megachile rotundata. Anim Behav 79:165–171CrossRefGoogle Scholar
  46. Roth LM (1948) A study of mosquito behavior. An experimental laboratory study of the sexual behavior of Aedes aegypti (Linnaeus). Am Midl Nat 40:265–352CrossRefGoogle Scholar
  47. Sakurai G, Kasuya E (2008) The costs of harassment in the adzuki bean beetle. Anim Behav 75:1367–1373CrossRefGoogle Scholar
  48. Scott TW, Chow E, Strickman D, Kittayapong P, Wirtz RA, Lorenz LH, Edman JD (1993) Blood-feeding patterns of Aedes aegypti (Diptera: Culicidae) collected in a rural Thai village. J Med Entomol 30:922–927PubMedGoogle Scholar
  49. Scott TW, Amerasinghe PH, Morrison AC, Lorenz LH, Clark GG, Strickman D, Kittayapong P, Edman JD (2000) Longitudinal studies of Aedes aegypti (Diptera: Culicidae) in Thailand and Puerto Rico: blood feeding frequency. J Med Entomol 37:89–101PubMedCrossRefGoogle Scholar
  50. 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 24:91–94PubMedCrossRefGoogle Scholar
  51. Spielman A (1964) The mechanics of copulation in Aedes aegypti. Biol Bull 127:324–344CrossRefGoogle Scholar
  52. Styer LM, Minnick SL, Sun AK, Scott TW (2007) Mortality and reproductive dynamics of Aedes aegypti (Diptera: Culicidae) fed human blood. Vector Borne Zoonotic Dis 7:86–98PubMedCrossRefGoogle Scholar
  53. 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 68:1–5PubMedGoogle Scholar
  54. Watson PJ, Arnqvist G, Stallmann RR (1998) Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 151:46–58PubMedCrossRefGoogle Scholar
  55. Wendell MD, Wilson TG, Higgs S, Black WC (2000) Chemical and gamma-ray mutagenesis of the white gene in Aedes aegypti. Insect Mol Biol 9:119–125PubMedCrossRefGoogle Scholar
  56. Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Philos Trans R Soc Lond B 364:1107–1115CrossRefGoogle Scholar
  57. Wolfner MF (1997) Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol 27:179–192PubMedCrossRefGoogle Scholar
  58. Yuval B (2006) Mating systems of blood-feeding flies. Ann Rev Entomol 51:413–440CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Michelle E. H. Helinski
    • 1
  • Laura C. Harrington
    • 1
  1. 1.Department of EntomologyCornell UniversityIthacaUSA

Personalised recommendations