Behavioral Ecology and Sociobiology

, Volume 67, Issue 6, pp 937–946 | Cite as

Elucidating the function of ejaculate expulsion and consumption after copulation by female Euxesta bilimeki

  • Christian Luis Rodriguez-Enriquez
  • Eduardo Tadeo
  • Juan Rull
Original Paper

Abstract

Postcopulatory processes can influence male reproductive success in several animal species. Females can use different mechanisms to bias male paternity after copulation. One of such mechanisms consists in expelling all or part of the ejaculate after copulation. Euxesta bilimeki is an Ulidiid fly whose females not only frequently expel ejaculates after mating but also consume the ejaculate after expulsion. In order to understand the significance of these behaviors we examined video recordings of courtship, copulatory, and postcopulatory behaviours. The presence of sperm in female storage organs was confirmed after mating with males of different sizes and was correlated with duration of courtship, copulation, and the period from the end of copulation to ejaculate expulsion. The effect of ejaculate consumption on female fitness (fecundity and longevity) was compared among females held under different dietary treatments: a rich diet consisting of protein, sugar and water, an intermediate diet composed of sugar and water, a poor diet of only water and females that were completely deprived of food and water. All of the observed females expelled ejaculates after mating. The probability of storing sperm in the two spermathecae and the ventral receptacle was correlated with interactions between the duration of all behaviours examined and male size. Except for starved females, who lived longer when allowed to consume ejaculates, ejaculate consumption had no effect on fitness. Results suggest that females can bias sperm storage according to male mating effort, while the consumed ejaculate had some nutritional value only evident when females were completely starved.

Keywords

Ejaculate expulsion Ejaculate consumption Cryptic female choice Courtship Nuptial gift Female fitness 

Supplementary material

ESM 1

(WMV 1631 kb)

ESM 2

(WMV 2476 kb)

References

  1. Aluja M, Rull J, Sivinski J, Trujillo G, Pérez-Staples D (2009) Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. J Insect Physiol 55:1091–1098PubMedCrossRefGoogle Scholar
  2. Andersson M, Simmons L (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedCrossRefGoogle Scholar
  3. Arnqvist G, Rowe L (2005) Sexual conflict. Princeton Univ. Press, New JerseyGoogle Scholar
  4. Bonduriansky R (2003) Layered sexual selection: a comparative analysis of sexual behaviour within an assemblage of piophilid flies. Can J Zool 81:479–491CrossRefGoogle Scholar
  5. Bonduriansky R, Brooks R (1998) Male antler flies (Protopiophila litigata; Diptera: Piophilidae) are more selective than females in mate choice. Can J Zool 76:1277–1285Google Scholar
  6. Bonduriansky R, Wheeler J, Rowe L (2005) Ejaculate feeding and female fitness in the sexually dimorphic fly Prochyliza xanthostoma (Diptera: Piophilidae). Anim Behav 69:489–497CrossRefGoogle Scholar
  7. Brunel O, Rull J (2010) The natural history and unusual mating behavior of Euxesta bilimeki (Diptera: Ulidiidae). Ann Entomol Soc Am 103:111–119CrossRefGoogle Scholar
  8. Burger M (2007) Sperm dumping in a haplogyne spider. J Zool 273:74–81CrossRefGoogle Scholar
  9. Burger M (2010) Complex female genitalia indicate sperm dumping in armored goblin spiders (Arachnida, Araneae, Oonopidae). Zoology 113:19–32PubMedCrossRefGoogle Scholar
  10. Chapman T, Arnqvist G, Bangham J, Rowe L (2003) Sexual conflict. Trends Ecol Evol 18:41–47CrossRefGoogle Scholar
  11. Clutton-Brock T, Langley P (1997) Persistent courtship reduces male and female longevity in captive tsetse flies Glossina morsitans morsitans Westwood (Diptera: Glossinidae). Behav Ecol 8:392CrossRefGoogle Scholar
  12. Cordts R, Partridge L (1996) Courtship reduces longevity of male Drosophila melanogaster. Anim Behav 52:269–278CrossRefGoogle Scholar
  13. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  14. Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, UKGoogle Scholar
  15. Dean R, Nakagawa S, Pizzari T (2011) The risk and intensity of sperm ejection in female birds. Am Nat 178:343–354PubMedCrossRefGoogle Scholar
  16. deCarvalho TN, Shaw KL (2005) Nuptial feeding of spermless spermatophores in the Hawaiian swordtail cricket, Laupala pacifica (Gryllidae: Triginodiinae). Naturwissenschaften 92:483–487PubMedCrossRefGoogle Scholar
  17. Drew RAI, Yuval B (2000) The evolution of fruit fly feeding behavior. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC, Boca Raton, FL, pp 731–749Google Scholar
  18. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton Univ Press, UKGoogle Scholar
  19. Eberhard W (2009) Postcopulatory sexual selection: Darwin's omission and its consequences. Proc Natl Acad Sci U S A 106(Supplement 1):10025PubMedCrossRefGoogle Scholar
  20. Eberhard WG, Pereira F (1995) The process of intromission in the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidiae). Psyche 102:99–120CrossRefGoogle Scholar
  21. Edvardsson M (2007) Female C allosobruchus maculatus mate when they are thirsty: resource-rich ejaculates as mating effort in a beetle. Anim Behav 74:183–188CrossRefGoogle Scholar
  22. Edvardsson M, Arnqvist G (2000) Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum. Proc R Soc Lond B Biol Sci 267:559–563CrossRefGoogle Scholar
  23. Gentry HS (1982) Agaves of continental North America. Univ. of Arizona Press, ArizonaGoogle Scholar
  24. Gwynne DT (1993) Food quality controls sexual selection in Mormon crickets by altering male mating investment. Ecology 74:1406–1413CrossRefGoogle Scholar
  25. Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101Google Scholar
  26. Hamm AH (1933) The epigamic behaviour and courtship of three species of Empididae. Entomol Mon Mag 69:113–117Google Scholar
  27. Hass B (1990) A quantitative study of insemination and gamete efficiency in different species of the Rhabditis strongyloides group (Nematoda). Invert Reprod Develop 18:205–208CrossRefGoogle Scholar
  28. Helfenstein F, Wagner RH, Danchin E (2003) Sexual conflict over sperm ejection in monogamous pairs of kittiwakes Rissa tridactyla. Behav Ecol Sociobiol 54:370–376CrossRefGoogle Scholar
  29. Irwin JT, Lee RE (2000) Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol 46:655–661PubMedCrossRefGoogle Scholar
  30. Ivy TM, Johnson JC, Sakaluk SK (1999) Hydration benefits to courtship feeding in crickets. Proc Roy Soc B 266:1523–1527CrossRefGoogle Scholar
  31. Kaitala A, Wiklund C (1995) Female mate choice and mating cost in the polyandrous butterfly Pieris napi (Lepidoptera, Pieridae). J Insect Behav 8:355–363CrossRefGoogle Scholar
  32. Kessel EL (1955) Mating activities of balloon flies. Syst Zool 4:97–104CrossRefGoogle Scholar
  33. LeBas NR, Hockham LR (2005) An invasion of cheats: the evolution of worthless nuptial gifts. Curr Biol 15:64–67PubMedGoogle Scholar
  34. Lorch PD, Wilkinson GS, Reillo PR (1993) Copulation duration and sperm precedence in the stalk-eyed fly Cyrtodiopsis whitei (Diptera: Diopsidae). Behav Ecol Sociobiol 32:303–311CrossRefGoogle Scholar
  35. Manier M, Belote J, Berben K, Novikov D, Stuart W, Pitnick S (2010) Resolving mechanisms of competitive fertilization success in Drosophila melanogaster. Science 328(5976):354PubMedCrossRefGoogle Scholar
  36. Otronen M, Siva-Jothy M (1991) The effect of postcopulatory male behaviour on ejaculate distribution within the female sperm storage organs of the fly, Dryomyza anilis (Diptera: Dryomyzidae). Behav Ecol Sociobiol 29:33–37CrossRefGoogle Scholar
  37. Parker G (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  38. Parker G (2006) Sexual conflict over mating and fertilization: an overview. Phil Trans Roy Soc Lond B 361:235–259CrossRefGoogle Scholar
  39. Parker GA, Simmons LW (1994) Evolution of phenotypic optima and copula duration in dungflies. Nature 370:53–56CrossRefGoogle Scholar
  40. Peretti A, Eberhard W (2009) Cryptic female choice via sperm dumping favours male copulatory courtship in a spider. J Evol Biol 23:271–281CrossRefGoogle Scholar
  41. Perez-Staples D, Harmer A, Taylor P (2007) Sperm storage and utilization in female Queensland fruit flies (Bactrocera tryoni). Phys Ent 32:127–135CrossRefGoogle Scholar
  42. Pizzari T, Birkhead T (2000) Female feral fowl eject sperm of subdominant males. Nature 405:787–789PubMedCrossRefGoogle Scholar
  43. Preston-Mafham KG (1999) Courtship and mating in Empis (Xanthempis) trigramma Meig., E-tessellata F. and E. (Polyblepharis) opaca F. (Diptera: Empididae) and the possible implications of 'cheating' behaviour. J Zool 247:239–246Google Scholar
  44. Rehfeld V, Sudhaus W (1985) Comparative studies of sexual behavior of two sibling species of Rhabditis (Nematoda). Zool Jb Syst 112:435–454Google Scholar
  45. Rodriguez V, Windsor D, Eberhard W (2004) Tortoise beetle genitalia and demonstration of a sexually selected advantage for flagellum length in Chelymorpha alternans (Chrysomelidae, Cassidinae, Stolaini). In: Jolivet P, Santiago-Blay JA, Schmitt M (eds) New developments in the biology of Chrysomelidae. SPB Academic Publishing, The Hague, pp 739–748Google Scholar
  46. Sadowski JA, Moore AJ, Brodie ED III (1999) The evolution of empty nuptial gifts in a dance fly (Diptera: Empididae): bigger isn’t always better. Behav Ecol Sociobiol 45:161–166CrossRefGoogle Scholar
  47. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst :125–146Google Scholar
  48. Siva-Jothy MT, Tsubaki Y (1989) Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae). Behav Ecol Sociobiol 25:261–267CrossRefGoogle Scholar
  49. Snook RR, Hosken DJ (2004) Sperm death and dumping in Drosophila. Nature 428:939–941PubMedCrossRefGoogle Scholar
  50. Taylor P, Kaspi R, Yuval B (2000) Copula duration and sperm storage in Mediterranean fruit flies from a wild population. Physiol Entomol 25:94–99CrossRefGoogle Scholar
  51. Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788Google Scholar
  52. Ursprung C, Den Hollander M, Gwynne DT (2009) Female seed beetles, Callosobruchus maculatus, remate for male-supplied water rather than ejaculate nutrition. Behav Ecol Sociobiol 63:781–788CrossRefGoogle Scholar
  53. Vahed K (1998) The function of nuptial feeding in insects: a review of empirical studies. Biol Rev 73:43–78CrossRefGoogle Scholar
  54. Vahed K (2007) All that glisters is not gold: sensory bias, sexual conflict and nuptial feeding in insects and spiders. Ethology 113:105–127CrossRefGoogle Scholar
  55. Wagner RH, Helfenstein F, Danchin E (2004) Female choice of young sperm in a genetically monogamous bird. Proc R Soc Lond B 271:S134CrossRefGoogle Scholar
  56. Warwick S, Vahed K, Raubenheimer D, Simpson SJ (2009) Free amino acids as phagostimulants in cricket nuptial gifts: support for the ‘Candymaker’ hypothesis. Biology letters 5:194–196Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Christian Luis Rodriguez-Enriquez
    • 1
  • Eduardo Tadeo
    • 1
  • Juan Rull
    • 1
  1. 1.Instituto de Ecología, A.C.XalapaMexico

Personalised recommendations