Journal of Insect Behavior

, Volume 14, Issue 3, pp 385–399 | Cite as

A Potential Cost of Monandry in the Lekking Sandfly Lutzomyia Longipalpis



Multiple mating by females is a subject of considerable controversy. In some species, however, females appear to mate only once, and the potential costs and benefits of this behavior are equally intriguing. When male mating success is highly skewed, monandrous females potentially risk mating with a sperm depleted male. In lek-breeding species, a male may gain up to 80% of available matings, yet few studies have explored whether these highly successful males suffer sperm depletion. These points are investigated in a series of laboratory experiments on the lekking sandfly, Lutzomyia longipalpis. It is shown that females may actively reject males prior to and after genital contact and that mated females do not remate within a single egg-laying cycle regardless of the refractory period between the first and subsequent matings. Males mate multiply and suffer from the effects of sperm depletion after their fifth copulation. Despite this, they continue to court and copulate females with equal vigor and females do not appear to detect sperm-depleted males: they lay similar numbers of eggs irrespective of the number of females their mate has previously copulated with. The implications of a single mating for L. longipalpis females in natural and laboratory leks are discussed.

monandry lekking sandfly sperm depletion 


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  1. Alatalo, R. V., Burke, T., Dann, J., Hanotte, O., Höglund, J., Lundberg, A., Moss, R., and Rintamaki, P. T. (1996). Paternity, copulation disturbance and female choice in lekking black grouse. Anim. Behav. 52: 861-873.Google Scholar
  2. Bateman, P. W. (1998). Mate preference for novel partners in the cricket Gryllus bimaculatus. Ecol. Entomol. 23: 473-475.Google Scholar
  3. Chaniotis, B. N. (1967). The biology of California Phlebotomus (Diptera: Psychodidae) under laboratory conditions. J. Med. Entomol. 4: 221-233.PubMedGoogle Scholar
  4. Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F., and Partridge, L. (1995). Cost of mating in Drosophila melanogaster females is mediated by male accessory-gland products. Nature 373: 241-244.PubMedGoogle Scholar
  5. Clutton-Brock,T., and Langley, P. (1997). Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Behav. Ecol. 8: 392-395.Google Scholar
  6. Cook, P. A. (1999). Sperm numbers and female fertility in the moth Plodia interpunctella (Hubner) (Lepidoptera; Pyralidae). J. Insect Behav. 12: 767-779.Google Scholar
  7. Dye, C., Davies, C. R., and Lainson, R. (1991). Communication among phlebotomine sandflies: A field study of domesticated Lutzomyia longipalpis populations in Amazonian Brazil. Anim. Behav. 42: 183-192.Google Scholar
  8. Eady, P. E. (1995). Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav. Ecol. Sociobiol. 36: 25-32.Google Scholar
  9. Flecknell, P. A. (1987). Laboratory Animal Anesthesia, Academic Press, London.Google Scholar
  10. Fox, C.W., Hickman, D. L., Raleigh, E. L., and Mousseau, T. A. (1995). Paternal investment in a seed beetle (Coleoptera, Bruchidae): Influence of male size, age and mating history. Ann. Entomol. Soc. Am. 88: 100-103.Google Scholar
  11. Hayashi, F. (1998). Multiple mating and lifetime reproductive output in female dobsonflies that receive nuptial gifts. Ecol. Res. 13: 283-289.Google Scholar
  12. Hosken, D. J., and Blanckenhorn, W. U. (1999). Female multiple mating, inbreeding avoidance, and fitness: It is not only the magnitude of costs and benefits that counts. Behav. Ecol. 10: 462-464.Google Scholar
  13. Hou, M. L., and Sheng, C. F. (1999). Fecundity and longevity of Helicoverpa armigera (Lepidoptera: Noctuidae): Effects of multiple mating. J. Econ. Entomol. 92: 569-573.Google Scholar
  14. Hughes, L., Chang, B. S. W., Wagner, D., and Pierce, N. E. (2000). Effects of mating history on ejaculate size, fecundity, longevity, and copulation duration in the anttended lycaenid butterfly, Jalmenus evagoras. Behav. Ecol. Sociobiol. 47: 119-128.Google Scholar
  15. Hurst, G. D. D., Sharpe, R. G., Broomfield, A. H., Walker, L. E., Majerus, T. M. O., Zakhorov, I. A., and Majerus, M. E. N. (1995). Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecol. Entomol. 20: 230-236.Google Scholar
  16. Höglund, J., and Alatalo, R. V. (1995). Leks, Monographs in Behavior and Ecology. Princeton University Press, Princeton, NJ.Google Scholar
  17. Imhof, M., Harr, B., Brem, G., and Schlotterer, C. (1998). Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol. Ecol. 7: 915-917.PubMedGoogle Scholar
  18. Jarvis, E. K., and Rutledge, L. C. (1992). Laboratory observations on mating and lek-like aggregations in Lutzomyia longipalpis (Diptera: Psychodidae). J. Med. Entomol. 29: 171-177.PubMedGoogle Scholar
  19. Jennions, M. D., and Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biol. Rev. Cambr. Phil. Soc. 75: 21-64.Google Scholar
  20. Johnstone, R. A., and Keller, L. (2000). How males can gain by harming their mates: Sexual conflict, seminal toxins, and the cost of mating. Am. Nat. 4: 368-377.Google Scholar
  21. Jones, T. M. (1997). Sexual Selection in the Sandfly Lutzomyia longipalpis, Ph. D. thesis, University of London, London.Google Scholar
  22. Jones, T. M., Quinnell, R. J., and Balmford, A. (1998) Fisherian flies: Benefits of female choice in a lekking sandfly. Proc. R. Soc. Lond. 265: 1651-1657.Google Scholar
  23. Jones, T. M., Balmford, A., and Quinnell, R. J. (2000). Adaptive female choice for middle-aged mates in a lekking sandfly. Proc. R. Soc. Lond. B 267: 681-686.PubMedGoogle Scholar
  24. Kellogg, K. A., Markert, J. A., Stauffer, J. R., and Kocher, T. D. (1995). Microsatellite variation demonstrates multiple paternity in lekking in cichlid fishes from Lake Malawi, Africa. Proc. R. Soc. Lond. 260: 79-84.Google Scholar
  25. Killick-Kendrick, R., Leaney, A. J., and Ready, P. D. (1977). The establishment, maintenance and productivity of a laboratory colony of Lutzomyia longipalpis (Diptera: Psychodidae). J. Med. Entomol. 13: 429-440.PubMedGoogle Scholar
  26. Lanctot, R. B., Scribner, K. T., Kempenaers, B., and Weatherhead, P. J. (1997). Lekking without a paradox in the buff-breasted sandpiper. Am. Nat. 149: 1051-1070.Google Scholar
  27. LaMunyon, C. W. (1997) Increased fecundity, as a function of multiple mating, in an arctiid moth, Utetheisa ornatrix. Ecol. Entomol. 22: 69-73.Google Scholar
  28. Lorch, P.D., Wilkinson, G. S., and Reillo, P. R. (1993). Copulation duration and sperm precedence in the stalk-eyed fly Cyrtodiopsis whitei (Diptera: diopsidae). Behav. Ecol. Sociobiol. 32: 303-311.Google Scholar
  29. Magnhagen, C. (1991). Predation risk as a cost of reproduction. Trends Ecol. Evol. 6: 183-185.Google Scholar
  30. Mair, J., and Blackwell, A. (1998). Effect of age and multiple mating on the mating behavior of Culicoides nubeculosus (Diptera: Ceratopogonidae). J. Med. Entomol. 35: 996-1001.PubMedGoogle Scholar
  31. Maroli, M., Bettini, S., Tricoli, D., Koury, C., and Perrotti, E. (1991). Studies on mating plug of two sandfly species, Phlebotomus pernisciosus and Phlebotomus papatasi (Diptera: Psychodidae). Parasitology 33: 405-411.Google Scholar
  32. Mbata, G. N., Shu, S. Q., and Ramaswamy, S. B. (1997). Rhythmicity of mating and oviposition in Callosobruchus subinnotatus (Pic) (Coleoptera: Bruchidae). J. Insect Behav. 10: 409-423.Google Scholar
  33. Nakatsuru, K., and Kramer, D. (1982). Is sperm cheap? Limited male fertility and female choice in the lemon tetra (Pisces, Characidae). Science 216: 753-755Google Scholar
  34. Ofuya, T. I. (1995). Multiple mating and its consequences in males of Callosobruchus maculatus (F) (Coleoptera, bruchidae). J. Stored Prod. Res. 31: 71-75.Google Scholar
  35. Olsson, M., and Madsen, T. (1995). Female choice on quantitative traits in lizards-Why is it so rare? Behav. Ecol. Sociobiol. 36: 179-184.Google Scholar
  36. Quinnell, R. J., and Dye, C. (1994). An experimental study of the peridomestic distribution of Lutzomyia longipalpis (Diptera: Psychodidae). Bull. Entomol. Res. 84: 379-382.Google Scholar
  37. Radwan, J., and Rysinksa, M. (1999). Effect of mating frequency on female fitness in Caloglyphus berlesei (Astigmata: Acaridae). Exp. Appl. Acarol. 23: 399-409.Google Scholar
  38. Reinhardt, K., Kohler, G., and Schumacher, J. (1999). Females of the grasshopper Chorthippus parallelus (Zett. ) do not remate for fresh sperm. Proc. R. Soc. Lond B 266: 2003-2009.Google Scholar
  39. Rice, W. (1989). Analyzing tables of statistical tests. Evolution 43: 223-225.Google Scholar
  40. Ridley, M. (1988). Mating frequency and fecundity in insects. Biol. Rev. Cambr. Phil. Soc. 63: 509-549.Google Scholar
  41. Rowe, L. (1994). The cost of mating and mate choice in water striders. Anim. Behav. 48: 1049-1056.Google Scholar
  42. Sakurai, T. (1996). Multiple mating and its effect on female reproductive output in the bean bug Reptortus clavatus (Heteroptera: Alydidae). Ann. Entomol. Soc. Am. 89: 481-485.Google Scholar
  43. Savalli, U. M., and Fox, C.W. (1999). The effect of male size, age, and mating behavior on sexual selection in the seed beetle Callosobruchus maculatus. Ethol. Ecol. Evol. 11: 49-60.Google Scholar
  44. Shine, R., Olsson, M. M., and Mason, R. T. (2000). Chastity belts in gartersnakes: The functional significance of mating plugs. Biol. J. Linn. Soc. 70: 377-390.Google Scholar
  45. Simmons, L. W. (1991). On the post-copulatory guarding behaviour of male field crickets. Anim. Behav. 42: 504-505Google Scholar
  46. Steele, R. H. (1984). An Investigation of Male Mating Success in Drosophila subobscura, Ph. D. thesis, University of Edinburgh, Edinburgh.Google Scholar
  47. Takakura, K. (1999). Active female courtship behavior and male nutritional contribution to female fecundity in Bruchidius dorsalis (Fahraeus) (Coleoptera: Bruchidae). Res.Pop. Ecol. 41: 269-273.Google Scholar
  48. Thornhill, R., and Alcock, J. (1983). Sexual Selection Theory, Harvard University Press, Cambridge, MA.Google Scholar
  49. Valenta, D. T., Killick-Kendrick, R., and Killick-Kendrick, M. (2000). Courtship and mating by the sandfly Phlebotomus duboscqi, a vector of zoonotic cutaneous leishmaniasis in the Afrotropical region. Med. Vet. Entomol. 14: 207-212.PubMedGoogle Scholar
  50. Westneat, D. F., and Rambo, T. B. (2000). Copulation exposes female Red-winged Blackbirds to bacteria in male semen. J. Avian Biol. 31: 1-7.Google Scholar
  51. Widemo, F., and Owens, I. P. F. (1995). Lek size, male mating skew and the evolution of lekking. Nature 373: 148-151.Google Scholar
  52. Wilson, N., Tufton, T. J., and Eady, P. E. (1999). The effect of single, double, and triple matings on the lifetime fecundity of Callosobruchus analis and Callosobruchus maculatus (Coleoptera: Bruchidae). J. Insect Behav. 12: 295-306.Google Scholar
  53. Yasui, Y. (1997). A “good-sperm” model can explain the evolution of costly multiple mating by females. Am. Nat. 149: 573-584.Google Scholar
  54. Yasui, Y. (1998). The 'genetic benefits' of female multiple mating reconsidered. Trends Ecol. Evol. 13: 246-250.Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  1. 1.Institute of ZoologyLondonUK
  2. 2.London School of Hygiene and Tropical MedicineLondonUK

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