Evolutionary Ecology

, Volume 21, Issue 1, pp 49–61 | Cite as

Nuptial gift consumption influences female remating in a scorpionfly: male or female control of mating rate?

  • Leif Engqvist
Original Paper


In the scorpionfly Panorpa cognata, males provide females with saliva secretions as nuptial food gifts. Consequently, females derive material benefits and possibly also genetic benefits from multiple matings. Females therefore generally should have a high motivation to remate. Males, on the other hand, do not share this interest, which will generate a sexual conflict over remating interval, possibly leading to male adaptations that prevent females from remating with other males. In this study, I found that mated females were less prone to copulate than virgin females, despite female benefits of multiple matings. Further, I found that the remating interval was significantly longer if the first copulation was long compared to shorter matings. This effect does not entirely depend on copulation duration per se, but on the amount of saliva, that a female is consuming during copulation. These results suggest a mating-induced refractory period and can be interpreted as male manipulation of female remating behaviour mediated through substances in the nuptial gift. Alternatively, receiving large nuptial gifts may decrease the prospective direct fitness benefits from further copulations, and thus change optimal female remating rate. Furthermore, gift size has been shown to correlate with male nutritional condition, which may be an indicator of male genetic quality. Females may therefore benefit indirectly by not remating following copulations involving large saliva gifts. In this scenario, female remating interval would be an effect of cryptic female choice.


Cryptic female choice Mecoptera Nuptial food gifts Panorpa Postcopulatory sexual selection Sexual conflict Sperm competition 


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I thank Joachim Frommen, Roger Härdling and two anonymous reviewers for helpful comments on the manuscript and Kim Schmidt, Nicole Schmidt and Monika Kräling for help with laboratory work. This study was supported by the Deutsche Forschungsgemeinschaft [EN 469/1-1].


  1. Alatalo RV, Kotiaho J, Mappes J, Parri S (1998) Mate choice for offspring performance: major benefits or minor costs? Proc R Soc Lond B 265:2297–2301CrossRefGoogle Scholar
  2. Alcock J (1994) Postinsemination associations between males and females in insects: the mate-guarding hypothesis. Annu Rev Entomol 39:1–21CrossRefGoogle Scholar
  3. Andersson J, Borg-Karlson AK, Wiklund C (2000) Sexual cooperation and conflict in butterflies: a male-transferred anti-aphrodisiac reduces harassment of recently mated females. Proc R Soc Lond B 267:1271–1275CrossRefGoogle Scholar
  4. Andersson J, Borg-Karlson AK, Wiklund C (2004) Sexual conflict and anti-aphrodisiac titre in a polyandrous butterfly: male ejaculate tailoring and absence of female control. Proc R Soc Lond B 271:1765–1770CrossRefGoogle Scholar
  5. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164PubMedCrossRefGoogle Scholar
  6. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University Press, PrincetonGoogle Scholar
  7. Baer B, Morgan ED, Schmid-Hempel P (2001) A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. Proc Natl Acad Sci USA 98:3926–3928PubMedCrossRefGoogle Scholar
  8. Bernays EA, Simpson SJ (1982) The control of food intake. Adv Insect Physiol 16:59–118CrossRefGoogle Scholar
  9. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefGoogle Scholar
  10. Bockwinkel G, Sauer KP (1994) Resource dependence of male mating tactics in the scorpionfly, Panorpa vulgaris (Mecoptera, Panorpidae). Anim Behav 47:203–209CrossRefGoogle Scholar
  11. Brown WD (1997) Female remating and the intensity of female choice in black-horned tree crickets, Oecanthus nigricornis. Behav Ecol 8:66–74CrossRefGoogle Scholar
  12. Byers GW, Thornhill R (1983) Biology of the Mecoptera. Annu Rev Entomol 28:203–228CrossRefGoogle Scholar
  13. Chapman T, Miyatake T, Smith HK, Partridge L (1998) Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc R Soc Lond B 265:1879–1894CrossRefGoogle Scholar
  14. Chen PS (1984) The functional-morphology and biochemistry of insect male accessory-glands and their secretions. Annu Rev Entomol 29:233–255CrossRefGoogle Scholar
  15. Cook PA, Gage MJG (1995) Effects of risks of sperm competition on the numbers of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera, Pyralidae). Behav Ecol Sociobiol 36:261–268Google Scholar
  16. Cook PA, Wedell N (1999) Non-fertile sperm delay female remating. Nature 397:486CrossRefGoogle Scholar
  17. Dickinson JL (1986) Prolonged mating in the milkweed beetle Labidomera clivicollis clivicollis (Cleoptera: Chrysomelidae): a test of the “sperm loading” hypothesis. Behav Ecol Sociobiol 18:331–338CrossRefGoogle Scholar
  18. Dziuk PJ (1996) Factors that influence the proportion of offspring sired by a male following heterospermic insemination. Anim Reprod Sci 43:65–88CrossRefGoogle Scholar
  19. Eady PE (1995) Why do male Callosobruchus maculatus beetles inseminate so many sperm? Behav Ecol Sociobiol 36:25–32CrossRefGoogle Scholar
  20. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJGoogle Scholar
  21. Eberhard WG, Cordero C (1995) Sexual selection by cryptic female choice on male seminal products—a new bridge between sexual selection and reproductive physiology. Trends Ecol Evol 10:493–496CrossRefGoogle Scholar
  22. Engqvist L (2006) Females benefit from mating with different males in the scorpionfly Panorpa cognata. Behav Ecol 17:435–440CrossRefGoogle Scholar
  23. Engqvist L, Sauer KP (2001) Strategic male mating effort and cryptic male choice in a scorpionfly. Proc R Soc Lond B 268:729–735CrossRefGoogle Scholar
  24. Engqvist L, Sauer KP (2002) Amorous scorpionflies: causes and consequences of the long pairing prelude of Panorpa cognata. Anim Behav 63:667–675CrossRefGoogle Scholar
  25. Engqvist L, Sauer KP (2003a) Determinants of sperm transfer in the scorpionfly Panorpa cognata: male variation, female condition and copulation duration. J Evol Biol 16:1196–1204CrossRefGoogle Scholar
  26. Engqvist L, Sauer KP (2003b) Influence of nutrition on courtship and mating behaviour in the scorpionfly Panorpa cognata. Ethology 109:911–928CrossRefGoogle Scholar
  27. Fleischman RR, Sakaluk SK (2004) Sexual conflict over remating in house crickets: no evidence of an anti-aphrodisiac in males’ ejaculates. Behaviour 141:633–646CrossRefGoogle Scholar
  28. Fox GA (2001) Failure-time analysis: emergence, flowering, survivorship, and other waiting times. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 253–289Google Scholar
  29. Härdling R, Kaitala A (2005) The evolution of repeated mating under sexual conflict. J Evol Biol 18:106–115PubMedCrossRefGoogle Scholar
  30. He Y, Tsubaki Y (1991) Effects of spermatophore size on female re-mating in the armyworm, Pseudoletia separata with reference to larval crowding. J Ethol 9:47–50CrossRefGoogle Scholar
  31. Holland B, Price WR (1998) Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1–7CrossRefGoogle Scholar
  32. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Statist 5:299–314CrossRefGoogle Scholar
  33. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  34. Johnson JC, Ivy TM, Sakaluk SK (1999) Female remating propensity contingent on sexual cannibalism in sagebrush crickets, Cyphoderris strepitans: a mechanism of cryptic female choice. Behav Ecol 10:227–233CrossRefGoogle Scholar
  35. Kirkpatrick M (1996) Good genes and direct selection in evolution of mating preferences. Evolution 50:2125–2140CrossRefGoogle Scholar
  36. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci USA 94:1282–1286PubMedCrossRefGoogle Scholar
  37. Leopold RA (1976) The role of male accessory glands in insect reproduction. Annu Rev Entomol 21:199–221CrossRefGoogle Scholar
  38. Lewis SM, Austad SN (1990) Sources of intraspecific variation in sperm precedence in red flour beetles. Am Nat 135:351–359CrossRefGoogle Scholar
  39. Mercier L (1915) Caractère sexuel secondaire chez les Panorpes: le rôle des glandes salivaires des males. Arch Zool Exp 55:1–5Google Scholar
  40. Miyatake T, Chapman T, Partridge L (1999) Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. J Insect Physiol 45:1021–1028PubMedCrossRefGoogle Scholar
  41. Møller AP, Jennions MD (2001) How important are direct fitness benefits of sexual selection? Naturwissenschaften 88:401–415PubMedCrossRefGoogle Scholar
  42. Oberhauser KS (1989) Effects of spermatophores on male and female monarch butterfly reproductive success. Behav Ecol Sociobiol 25:237–246CrossRefGoogle Scholar
  43. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567Google Scholar
  44. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sperm competition and the evolution of animal mating systems. Academic Press, New York, pp 1–60Google Scholar
  45. Parker GA, Simmons LW (1989) Nuptial feeding in insects: theoretical models of male and female interests. Ethology 82:3–26CrossRefGoogle Scholar
  46. Parker GA, Partridge L (1998) Sexual conflict and speciation. Philos Trans R Soc Lond B 353:261–274CrossRefGoogle Scholar
  47. Parker GA, Simmons LW, Kirk H (1990) Analysing sperm competition data: simple models for predicting mechanisms. Behav Ecol Sociobiol 27:55–65CrossRefGoogle Scholar
  48. Polak M, Wolf LL, Starmer WT, Barker JSF (2001) Function of the mating plug in Drosophila hibisci Bock. Behav Ecol Sociobiol 49:196–205CrossRefGoogle Scholar
  49. Sakaluk SK (1991) Post-copulatory mate guarding in decorated crickets. Anim Behav 41:207–216CrossRefGoogle Scholar
  50. Sakaluk SK, Eggert A-K (1996) Female control of sperm transfer and intraspecific variation in sperm. Evolution 50:694–703CrossRefGoogle Scholar
  51. Sakaluk SK, Avery RL, Weddle CB (2006) Cryptic sexual conflict in gift-giving insects: chasing the chase-away. Am Nat 167:94–104PubMedCrossRefGoogle Scholar
  52. Sauer KP (1970) Zur Monotopbindung einheimischer Arten der Gattung Panorpa (Mecoptera) nach Untersuchungen im Freiland und im Laboratorium. Zool Jahrb Syst 97:201–284Google Scholar
  53. Sauer KP (1977) The adaptive significance of genetic variability of photoperiodic response in Panorpa vulgaris. Zool Jahrb Syst 104:489–538Google Scholar
  54. Sauer KP, Lubjuhn T, Sindern J, Kullmann H, Kurtz J, Epplen C, Epplen JT (1998) Mating system and sexual selection in the scorpionfly Panorpa vulgaris (Mecoptera: Panorpidae). Naturwissenschaften 85:219–228CrossRefGoogle Scholar
  55. Sillén-Tullberg B (1981) Prolonged copulation—a male post-copulatory strategy in a promiscuous species, Lygaeus equestris (Heteroptera, Lygaeidae). Behav Ecol Sociobiol 9:283–289CrossRefGoogle Scholar
  56. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, NJGoogle Scholar
  57. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann Rev Ecol Evol Syst 36:125–146CrossRefGoogle Scholar
  58. Simmons LW, Parker GA (1989) Nuptial feeding in insects: mating effort versus paternal investment. Ethology 81:332–343Google Scholar
  59. Simmons LW, Gwynne DT (1991) The refractory period of female katydids (Orthoptera: Tettigonidae): sexual conflict over the remating interval? Behav Ecol 2:276–282CrossRefGoogle Scholar
  60. Simmons LW, Alcock J, Reeder A (2003) The role of cuticular hydrocarbons in male attraction and repulsion by female Dawson’s burrowing bee, Amegilla dawsoni. Anim Behav 66:677–685CrossRefGoogle Scholar
  61. Siva-Jothy MT, Stutt AD (2003) A matter of taste: direct detection of female mating status in the bedbug. Proc R Soc Lond B 270:649–652CrossRefGoogle Scholar
  62. Stockley P (1997) Sexual conflict resulting from adaptations to sperm competition. Trends Ecol Evol 12:154–159CrossRefGoogle Scholar
  63. Sugawara T (1979) Stretch reception in the bursa copulatrix of the butterfly, Pieris rapae crucivora, and its role in behavior. J Comp Physiol 130:191–199CrossRefGoogle Scholar
  64. Takakura K (2001) Courtship-role-reversal in the bean weevil, Bruchidius dorsalis (Coleoptera: Bruchidae): interplay between male-male competition and cryptic female choice. Appl Entomol Zoolog 36:311–316CrossRefGoogle Scholar
  65. Therneau TM, Grambsch PM (2004) Modeling survival data: extending the Cox model, 3rd edn. Springer, New YorkGoogle Scholar
  66. Thornhill R (1976) Sexual selection and nuptial feeding behaviour in Bittacus apicalis (Insecta: Mecoptera). Am Nat 110:529–548CrossRefGoogle Scholar
  67. Thornhill R (1979) Male pair-formation pheromones in Panorpa scorpionflies (Mecoptera: Panorpidae). Environ Entomol 8:886–888Google Scholar
  68. Thornhill R (1980) Competition and coexistence among Panorpa scorpionflies (Mecoptera: Panorpidae). Ecol Monogr 50:179–197CrossRefGoogle Scholar
  69. Thornhill R (1981) Panorpa (Mecoptera: Panorpidae) scorpionflies: systems for understanding resource-defense polygyny and alternative male reproductive efforts. Ann Rev Ecol Syst 12:355–386CrossRefGoogle Scholar
  70. Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788CrossRefGoogle Scholar
  71. Thornhill R, Sauer KP (1992) Genetic sire effects on the fighting ability of sons and daughters and mating success of sons in a scorpionfly. Anim Behav 43:255–264CrossRefGoogle Scholar
  72. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027PubMedCrossRefGoogle Scholar
  73. Tsubaki Y, Sokei Y (1988) Prolonged mating in the melon fly, Dacus cucurbitae (Diptera: Tephritidae): competition for fertilization by sperm-loading. Res Popul Ecol 30:343–352CrossRefGoogle Scholar
  74. Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43–78CrossRefGoogle Scholar
  75. Weddle CB, Sakaluk SK (2003) Ingestion of male haemolymph and mating propensity of female sagebrush crickets: no evidence of a male-derived antiaphrodisiac. Anim Behav 65:83–88CrossRefGoogle Scholar
  76. Wedell N (1993) Spermatophore size in bushcrickets: comparative evidence for nuptial gifts as a sperm protection device. Evolution 47:1203–1212CrossRefGoogle Scholar
  77. Wedell N (2005) Female receptivity in butterflies and moths. J exp Biol 208:3433–3440PubMedCrossRefGoogle Scholar
  78. Wedell N, Arak A (1989) The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigonidae, Decticus verrucivorus). Behav Ecol Sociobiol 24:117–125CrossRefGoogle Scholar
  79. Whitlock MC (2005) Combining probability from independent tests: the weighted Z-method is superior to Fisher’s approach. J Evol Biol 18:1368–1373PubMedCrossRefGoogle Scholar
  80. Wiklund C, Kaitala A (1995) Sexual selection for large male size in a polyandrous butterfly: the effect of body size on male versus female reproductive success in Pieris napi. Behav Ecol 6:6–13CrossRefGoogle Scholar
  81. Wiklund C, Karlsson B, Leimar O (2001) Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proc R Soc Lond B 268:1661–1667CrossRefGoogle Scholar
  82. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109:929–950CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Department of Evolutionary Biology and EcologyUniversity of BonnBonnGermany

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