Journal of Insect Behavior

, Volume 31, Issue 2, pp 144–157 | Cite as

Mating Status Effects on Sexual Response of Males and Females in the Parasitoid Wasp Urolepis rufipes

Article

Abstract

Although mate preferences are most commonly examined in females, they are often found in both sexes. In the parasitoid wasp Urolepis rufipes, both female and male mating status affected certain aspects of sexual interactions. Female mating status mattered only in the later stages of mating. Males did not discriminate between virgin and mated females in terms of which they contacted or mounted first. However, once mounted, most virgin females were receptive to copulation, whereas very few mated females were. Whether a male’s mating status affected his own sexual response depended on the female’s ability to respond and the stage of mating. Examining male behavior toward dead females allowed elimination of the role of female behavior in how males responded. Virgin and mated males are both attracted to dead females as evidenced by their fanning their wings at such females. However, mated males were quicker than virgin males to contact and to mount in an experiment with dead females, whereas there was no such differential response in an experiment with live females. This difference is consistent with greater female sexual responsiveness to virgin males. Male mating status also affected female receptivity to copulate. Once mounted, live virgin females were less likely to become receptive to copulation by mated males than to virgin males, but only in a choice experiment, not in a no-choice experiment.

Keywords

Mating history monandry parasitoid wasp receptivity virgin 

Notes

Acknowledgements

Thanks to K. Floate for U. rufipes; to A. Coletta, J. Niew and A. van Pelt for assistance with experiments; to J. Cooper. M. King, and W. Nichols for assistance with colony maintenance; and to A. Kremer for feedback on the writing.

References

  1. Ah-King M, Gowaty PA (2016) A conceptual review of mate choice: stochastic demography, within-sex phenotypic plasticity, and individual flexibility. Ecol Evol 6:4607–4642CrossRefPubMedPubMedCentralGoogle Scholar
  2. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164CrossRefPubMedGoogle Scholar
  3. Avila GA, Withers TM, Holwell GI (2017) Courtship and mating behaviour in the parasitoid wasp Cotesia urabae (hymenoptera: Braconidae): mate location and the influence of competition and body size on male mating success. Bull Entomol Res 107:439–447CrossRefPubMedGoogle Scholar
  4. Baeder JM, King BH (2004) Associative learning of color by males of the parasitoid wasp Nasonia vitripennis (hymenoptera: Pteromalidae). J Insect Behav 17:201–213CrossRefGoogle Scholar
  5. Boivin G (2013) Sperm as a limiting factor in mating success in hymenoptera parasitoids. Entomol Exp Appl 146:149–155CrossRefGoogle Scholar
  6. Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339CrossRefPubMedGoogle Scholar
  7. Boulton RA, Shuker DM (2015) The costs and benefits of multiple mating in a mostly monandrous wasp. Evolution 69:939–949.  https://doi.org/10.1111/evo.12636 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brent CS (2010) Reproduction of the western tarnished plant bug, Lygus hesperus, in relation to age, gonadal activity and mating status. J Insect Physiol 56:28–34CrossRefPubMedGoogle Scholar
  9. Bressac C, Thi Khanh HD, Chevrier C (2009) Effects of age and repeated mating on male sperm supply and paternity in a parasitoid wasp. Entomol Exp Appl 130:207–213CrossRefGoogle Scholar
  10. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  11. Cheng LI, Howard RW, Campbell JF, Charlton RE, Nechols JR, Ramaswamy SB (2004) Mating behavior of Cephalonomia tarsalis (Ashmead) (hymenoptera: Bethylidae) and the effect of female mating frequency on offspring production. J Insect Behav 17:227–245CrossRefGoogle Scholar
  12. Chirault M, Van de Zande L, Hidalgo K, Chevrier C, Bressac C, Lecureuil C (2016) The spatio-temporal partitioning of sperm by males of the prospermatogenic parasitoid Nasonia vitripennis is in line with its gregarious lifestyle. J Insect Physiol 91-92:10–17CrossRefPubMedGoogle Scholar
  13. Clausen CP (1939) The effect of host size upon the sex ratio of hymenopterous parasites and its relation to methods of rearing and colonization. J N Y Entomol Soc 47:1–9Google Scholar
  14. Cooper JL, King BH (2015) Substrate-borne marking in the parasitoid wasp Urolepis rufipes (hymenoptera: Pteromalidae). Environ Entomol 44:680–688CrossRefPubMedGoogle Scholar
  15. Cooper JL, Burgess ER IV, King BH (2013) Courtship behavior and detection of female receptivity in the parasitoid wasp Urolepis rufipes. J Insect Behav 26:745–761CrossRefGoogle Scholar
  16. Dougherty LR, Shuker DM (2014) The effect of experimental design on the measurement of mate choice: a meta-analysis. Behav Ecol.  https://doi.org/10.1093/beheco/aru125
  17. Fedorka K, Zuk M (2005) Sexual conflict and female immune suppression in the cricket, Allonemobious socius. J Evol Biol 18:1515–1522CrossRefPubMedGoogle Scholar
  18. Fischer CR, King BH (2008) Sexual inhibition in Spalangia endius males after mating and time for ejaculate replenishment. J Insect Behav 21:1–8CrossRefGoogle Scholar
  19. Fleischman R, Sakaluk SK (2004) Sexual conflict over remating in house crickets: no evidence of an anti-aphrodisiac in males' ejaculates. Behavior 141:633–646CrossRefGoogle Scholar
  20. Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. Biol Rev 82:26–48CrossRefGoogle Scholar
  21. Gerling D, Legner EF (1968) Developmental history and reproduction of Spalangia cameroni, parasite of synanthropic flies. Ann Entomol Soc Am 61:1436–1443CrossRefGoogle Scholar
  22. Gerofotis CD, Yuval B, Ioannou CS, Nakas CT, Papadopoulos NT (2015) Polygyny in the olive fly: effects on male and female fitness. Behav Ecol Sociobiol 69:1323–1332CrossRefGoogle Scholar
  23. Gershman SN (2008) Sex-specific differences in immunological costs of multiple mating in Gryllus vocalis field cricket. Behav Ecol 19:810–815CrossRefGoogle Scholar
  24. Geuverink E, Gerritsma S, Pannebakker BA, Beukeboom LW (2009) A role for sexual conflict in the evolution of reproductive traits in Nasonia wasps? Anim Biol 59:417–434.  https://doi.org/10.1163/157075509x12499949744261 CrossRefGoogle Scholar
  25. Gibson GAP, Floate KD (2004) Filth fly parasitoids; on dairy farms in Ontario and Quebec, Canada. Can Entomol 136:407–417CrossRefGoogle Scholar
  26. Godfray HCJ (1994) Parasitoids. Princeton University Press, PrincetonGoogle Scholar
  27. Grillenberger BK, Gadau J, Bijlsma R, Van De Zande L, Beukeboom LW (2009) Female dispersal and isolation-by-distance of Nasonia vitripennis populations in a local mate competition context. Entomol Exp Appl 132:147–154CrossRefGoogle Scholar
  28. Halliday T (1983) The study of mate choice. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 3–32Google Scholar
  29. Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488CrossRefPubMedGoogle Scholar
  30. Hardy ICW (1994) Sex ratio and mating structure in the parasitoid hymenoptera. Oikos 69:3–20CrossRefGoogle Scholar
  31. Heimpel GE, Lundgren JG (2000) Sex ratios of commercially reared biological control agents. Biol Control 19:77–93.  https://doi.org/10.1006/bcon.2000.0849 CrossRefGoogle Scholar
  32. Judge KA, Tran K-C, Gwynne DT (2010) The relative effects of mating status and age on the mating behaviour of female field crickets. Can J Zool 88:219–223CrossRefGoogle Scholar
  33. Kant R, Trewick SA, Sandanayaka WRM, Godfrey AJR, Minor MA (2012) Effects of multiple matings on reproductive fitness of male and female Diaeretiella rapae. Entomol Exp Appl 145:215-221Kemp DJ (2012) costly copulation in the wild: mating increases the risk of parasitoid-mediated death in swarming locusts. Behav Ecol 23:191–194.  https://doi.org/10.1093/beheco/arr173 CrossRefGoogle Scholar
  34. Kemp DJ (2012) Costly copulation in the wild: mating increases the risk of parasitoid-mediated death in swarming locusts. Behav Ecol 23:191–194.  https://doi.org/10.1093/beheco/arr173 CrossRefGoogle Scholar
  35. King BH (1993) Flight activity in the parasitoid wasp Nasonia vitripennis (hymenoptera: Pteromalidae). J Insect Behav 6:313–321CrossRefGoogle Scholar
  36. King BH (2002) Breeding strategies in females of the parasitoid wasp Spalangia endius: effects of mating status and body size. J Insect Behav 15:181–193CrossRefGoogle Scholar
  37. King BH, Kuban KA (2012) Should he stay or should he go: male influence on offspring sex ratio via postcopulatory attendance. Behav Ecol Sociobiol 66:1165–1173CrossRefGoogle Scholar
  38. King BH, Owen MA (2012) Post-mating changes in restlessness, speed and route directness in males of the parasitoid wasp Spalangia endius (hymenoptera: Pteromalidae). J Insect Behav 25:309–319CrossRefGoogle Scholar
  39. King BH, Saporito KB, Ellison JH, Bratzke RM (2005) Unattractiveness of mated females to males in the parasitoid wasp Spalangia endius. Behav Ecol Sociobiol 57:350–356CrossRefGoogle Scholar
  40. King BH, Colyott KL, Chesney AR (2014) Livestock bedding effects on two species of parasitoid wasps of filth flies. J Insect Sci 14:185CrossRefPubMedGoogle Scholar
  41. Leonard JE, Boake CRB (2006) Site-dependent aggression and mating behaviour in three species of Nasonia (hymenoptera: Pteromalidae). Anim Behav 71:641–647CrossRefGoogle Scholar
  42. Matthews JR, Petersen JJ (1990) Effects of host age, host density and parent age on reproduction of the filth fly parasite Urolepis rufipes (hymenoptera: Pteromalidae). Med Vet Entomol 4:255–260CrossRefPubMedGoogle Scholar
  43. McAllister BF, Werren JH (1997) Phylogenetic analysis of a retrotransposon with implications for strong evolutionary constraints on reverse transcriptase. Mol Biol Evol 14:69–80CrossRefPubMedGoogle Scholar
  44. McNamara K, Elgar M, Jones T (2008) A longevity cost of re-mating but no benefits of polyandry in the almond moth, Cadra cautella. Behav Ecol Sociobiol 62:1433–1440CrossRefGoogle Scholar
  45. Myint WW, Walter GH (1990) Behaviour of Spalangia cameroni males and sex ratio theory. Oikos 59:163–174CrossRefGoogle Scholar
  46. Noronha C, Gibson GAP, Floate KD (2007) Hymenopterous parasitoids of house fly and stable fly puparia in Prince Edward Island and New Brunswick, Canada. Can Entomol 139:748–750CrossRefGoogle Scholar
  47. Ortigosa A, Rowe L (2003) The role of mating history and male size in determining mating behaviours and sexual conflict in a water strider. Anim Behav 65:851–858CrossRefGoogle Scholar
  48. Powell JR, Graham LC, Galloway TD (2003) Development time of Urolepis rufipes (hymenoptera: Pteromalidae) and effect of female density on offspring sex ratio and reproductive output. Proc Entomol Soc Manitoba 59:16–20Google Scholar
  49. Pultz MA, Leaf DS (2003) The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis 35:185–191CrossRefPubMedGoogle Scholar
  50. Reumer BM, Kraaijeveld K, van Alphen JJM (2007) Selection in the absence of males does not affect male–female conflict in the parasitoid wasp Leptopilina clavipes (hymenoptera: Figitidae). J Insect Physiol 53:994–999.  https://doi.org/10.1016/j.jinsphys.2007.05.002 CrossRefPubMedGoogle Scholar
  51. Ridley M (1993) Clutch size and mating frequency in parasitic hymenoptera. Am Nat 142:893–910CrossRefGoogle Scholar
  52. Rueda LM, Axtell RC (1985) Guide to common species of pupal parasites (hymenoptera: Pteromalidae) of the house fly and other muscoid flies associated with poultry and livestock manure, technical bulletin 278. In: North Carolina Agricultural Research Service, North Carolina State University. http://www.nhm.ac.uk/resources/research-curation/projects/chalcidoids/pdf_Y/RuedaAx985.pdf
  53. Ruther J, Matschke M, Garbe LA, Steiner S (2009) Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis. Proc R Soc B Bio 276:3303–3310CrossRefGoogle Scholar
  54. Salehialavi Y, Fritzsche K, Arnqvist G (2011) The cost of mating and mutual mate choice in 2 role–reversed honey locust beetles. Behav Ecol 22:1104–1113CrossRefGoogle Scholar
  55. Santolamazza-Carbone S, Pestana M (2010) Polyandry increases male offspring production in the quasi-gregarious egg parasitoid Anaphes nitens. Ethol Ecol Evol 22:51–61.  https://doi.org/10.1080/03949370903515984 CrossRefGoogle Scholar
  56. Steiner S, Ruther J (2009) How important is sex for females of a haplodiploid species under local mate competition? Behav Ecol 20:570–574CrossRefGoogle Scholar
  57. Steiner S, Henrich N, Ruther J (2008) Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus. Entomol Exp Appl 126:131–137CrossRefGoogle Scholar
  58. van Alphen J, Bernstein C, Driessen G (2003) Information acquisition and time allocation in insect parasitoids. Trends Ecol Evol 18:81–87CrossRefGoogle Scholar
  59. Wang D, Lu L, He Y, Shi Q, Tu C, Gu J (2016) Mate choice and host discrimination behavior of the parasitoid Trichogramma chilonis. Bull Entomol Res 106:530–537CrossRefPubMedGoogle Scholar
  60. Wedell N, Gage M, Parker G (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320CrossRefGoogle Scholar
  61. West SA (2009) Sex allocation. Princeton University Press, PrincetonCrossRefGoogle Scholar
  62. Wittman TN (2016) Behavioral and chemical ecology of a male produced substrate borne pheromone in Urolepis rufipes. Thesis, Northern Illinois UniversityGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biological SciencesNorthern Illinois UniversityDeKalbUSA
  2. 2.Entomology DepartmentWatermanUSA

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