Behavioral Ecology and Sociobiology

, Volume 66, Issue 2, pp 181–190 | Cite as

Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

  • Arild Johnsen
  • Kim L. Carter
  • Kaspar Delhey
  • Jan T. Lifjeld
  • Raleigh J. Robertson
  • Bart Kempenaers
Original Paper

Abstract

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.

Keywords

Extra-pair paternity Sperm competition Fertility Sperm Copulation behaviour 

Notes

Acknowledgments

We thank Cheryl Bishop, Frode Fossøy, Karin Hieke, Terje Laskemoen, Anne Peters, Thomas Petitguyot, Angelika Poesel, Agnes Tuerk, Emmi Schlicht and Mihai Valcu for assistance in the field, and Frode Fossøy for lab assistance. We are grateful to Raphael-Thomas Klumpp and Alfred Fojt from the Institute of Silviculture, Vienna, for providing access to their facilities, to Hans Winkler from the Konrad Lorenz Institute for Comparative Ethology, Vienna, for logistical support, to the staff at the Queen’s University Biological Station for facilities and logistical support, and to Chris Eckert at Queens’ University for letting us use his microscopy laboratory. BK designed the study; KC and BK conducted the blue tit field work; AJ, KC, KD, JTL and BK conducted the bluethroat fieldwork; KC, RJR and BK conducted the tree swallow fieldwork; KC and BK counted the sperm on the egg membranes; KC conducted the blue tit paternity analysis, AJ conducted the bluethroat paternity analysis; AJ and BK analysed the data; AJ wrote the paper in collaboration with all other co-authors. We thank Jim Briskie and two anonymous reviewers for thoughtful comments on the manuscript. The work was funded by the Max Planck Society, the Norwegian research Council, the Natural History Museum of the University of Oslo, and the Natural Sciences and Engineering Research Council of Canada.

Ethical standards

The work described here was done under license and complied with the current laws of the countries in which it was performed.

Conflicts of interest

None

Supplementary material

265_2011_1265_MOESM1_ESM.doc (43 kb)
Table S1 Paternity of eggs (○ = within-pair, ● = extra-pair) in relation to laying order in blue tits (DOC 43 kb)
265_2011_1265_MOESM2_ESM.doc (44 kb)
Table S2 Paternity of eggs (○ = within-pair, ● = extra-pair, ? = unknown) in relation to laying order in bluethroats (DOC 44 kb)

References

  1. Barber CA, Robertson RJ (2007) Timing of copulations and the pattern of paternity in relation to laying order in tree swallows Tachycineta bicolor. J Avian Biol 38:249–254CrossRefGoogle Scholar
  2. Birkhead TR, Biggins JD (1998) Sperm competition mechansims in birds: models and data. Behav Ecol 9:253–287CrossRefGoogle Scholar
  3. Birkhead TR, Fletcher F (1995) Depletion determines sperm number in male zebra finches. Anim Behav 49:451–456CrossRefGoogle Scholar
  4. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic, LondonGoogle Scholar
  5. Birkhead TR, Petrie M (1995) Ejaculate features and sperm utilization in peafowl Pavo cristatus. Proc R Soc Lond B 261:153–158CrossRefGoogle Scholar
  6. Birkhead TR, Pellatt EJ, Fletcher F (1993) Selection and utilization of spermatozoa in the reproductive tract of the female zebra finch Taeniopygia guttata. J Reprod Fertil 99:593–600PubMedCrossRefGoogle Scholar
  7. Birkhead TR, Sheldon BC, Fletcher F (1994) A comparative study of sperm–egg interactions in birds. J Reprod Fertil 101:353–361PubMedCrossRefGoogle Scholar
  8. Birkhead TR, Wishart GJ, Biggins JD (1995) Sperm precedence in the domestic fowl. Proc R Soc Lond B 261:285–292CrossRefGoogle Scholar
  9. Charmantier A, Blondel J (2003) A contrast in extra-pair paternity levels on mainland and island populations of mediterranean blue tits. Ethology 109:351–363CrossRefGoogle Scholar
  10. Crowe SA, Kleven O, Delmore KE, Laskemoen T, Nocera JJ, Lifjeld JT, Robertson RJ (2009) Paternity assurance through frequent copulations in a wild passerine with intense sperm competition. Anim Behav 77:183–187CrossRefGoogle Scholar
  11. Delhey K, Johnsen A, Peters A, Andersson S, Kempenaers B (2003) Paternity analysis reveals opposing selection pressures on crown colouration in the blue tit (Parus caeruleus). Proc R Soc Lond B 270:2057–2063CrossRefGoogle Scholar
  12. Delhey K, Peters A, Johnsen A, Kempenaers B (2007) Fertilization success and UV ornamentation in blue tits Cyanistes caeruleus: correlational and experimental evidence. Behav Ecol 18:399–409CrossRefGoogle Scholar
  13. Denk AG, Holzmann A, Peters A, Vermeirssen ELM, Kempenaers B (2005) Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16:825–833CrossRefGoogle Scholar
  14. Double MC, Dawson D, Burke T, Cockburn A (1997) Finding the fathers in the least faithful bird: a microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol Ecol 6:691–693CrossRefGoogle Scholar
  15. Dunn P, Robertson R, Michaud-Freeman D, Boag P (1994) Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35:273–281CrossRefGoogle Scholar
  16. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton Univ. Press, Princeton, NJGoogle Scholar
  17. Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717PubMedCrossRefGoogle Scholar
  18. Fossøy F, Johnsen A, Lifjeld JT (2006) Evidence of obligate female promiscuity in a socially monogamous passerine. Behav Ecol Sociobiol 60:255–259CrossRefGoogle Scholar
  19. Fossøy F, Johnsen A, Lifjeld JT (2008) Multiple genetic benefits of promiscuity in a socially monogamous passerine. Evolution 62:145–156PubMedCrossRefGoogle Scholar
  20. Froman DP, Pizzari T, Feltmann AJ, Castillo-Juarez H, Birkhead T (2002) Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc R Soc Lond B 269:607–612CrossRefGoogle Scholar
  21. Griffith SC, Owens IPF, Thuman KA (2002) Extra-pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212PubMedCrossRefGoogle Scholar
  22. Johnsen A, Lifjeld JT (2003) Ecological constraints on extra-pair paternity in the bluethroat. Oecologia 136:476–483PubMedCrossRefGoogle Scholar
  23. Johnsen A, Andersen V, Sunding C, Lifjeld JT (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299PubMedCrossRefGoogle Scholar
  24. Johnsen A, Pärn H, Fossøy F, Kleven O, Laskemoen T, Lifjeld J (2008) Is female promiscuity constrained by the presence of her social mate? An experiment with bluethroats Luscinia svecica. Behav Ecol Sociobiol 62:1761–1767CrossRefGoogle Scholar
  25. Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496CrossRefGoogle Scholar
  26. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT (2009) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63:2466–2473PubMedCrossRefGoogle Scholar
  27. Krist M, Nadvornik P, Uvirova L, Bures S (2005) Paternity covaries with laying and hatching order in the collared flycatcher Ficedula albicollis. Behav Ecol Sociobiol 59:6–11CrossRefGoogle Scholar
  28. Krokene C, Lifjeld JT (2000) Variation in the frequency of extra-pair paternity in birds: a comparison of an island and a mainland population of blue tits. Behaviour 137:1317–1330CrossRefGoogle Scholar
  29. Krokene C, Anthonisen K, Lifjeld JT, Amundsen T (1996) Paternity and paternity assurance behaviour in the bluethroat, Luscinia s. svecica. Anim Behav 52:405–417CrossRefGoogle Scholar
  30. Krokene C, Rigstad K, Dale M, Lifjeld JT (1998) The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance? Behav Ecol 9:649–656CrossRefGoogle Scholar
  31. Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229CrossRefGoogle Scholar
  32. Lifjeld JT, Aas CK, Birkhead TR, Fletcher F, Krokene C, Rigstad K (2000) Variation in number of spermatozoa in blue tit and great tit eggs. Auk 117:246–249CrossRefGoogle Scholar
  33. Lifjeld JT, Johnsen A, Petitguyot T (2005) Egg-size variation in the bluethroat (Luscinia s. svecica): constraints and adaptation. J Ornithol 146:249–256CrossRefGoogle Scholar
  34. Magrath MJL, Vedder O, van der Velde M, Komdeur J (2009) Maternal effects contribute to the superior performance of extra-pair offspring. Curr Biol 19:792–797PubMedCrossRefGoogle Scholar
  35. Michl G, Török J, Griffith SC, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. Proc Natl Acad Sci USA 99:5466–5470PubMedCrossRefGoogle Scholar
  36. Pizzari T, Cornwallis CK, Løvlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74PubMedCrossRefGoogle Scholar
  37. Pryke SR, Rollins LA, Griffith SC (2010) Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science 329:964–967PubMedCrossRefGoogle Scholar
  38. Questiau S, Eybert M-C, Taberlet P (1999) Amplified fragment length polymorphism (AFLP) markers reveal extra-pair parentage in a bird species, the bluethroat (Luscinia svecica). Mol Ecol 8:1331–1339PubMedCrossRefGoogle Scholar
  39. Riley HT, Bryant DM, Carter RE, Parkin DT (1995) Extra-pair fertilizations and paternity defence in house martins, Delichon urbica. Anim Behav 49:495–509CrossRefGoogle Scholar
  40. Rudolfsen G, Figenschou L, Folstad I, Nordeide JT, Soreng E (2005) Potential fitness benefits from mate selection in the Atlantic cod (Gadus morhua). J Evol Biol 18:172–179PubMedCrossRefGoogle Scholar
  41. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  42. Small AO, Schlusser K, Ryan CJ, Jamieson IG (2000) Detecting sperm on the perivitelline membrane of incubated turkey eggs and its implications for research on fertility problems in endangered species. Wildlife Res 27:635–637CrossRefGoogle Scholar
  43. Stapleton MK, Robertson RJ (2006) Female tree swallow home-range movements during their fertile period as revealed by radio-tracking. Wilson J Ornithol 118:502–507CrossRefGoogle Scholar
  44. Stapleton MK, Kleven O, Lifjeld JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733CrossRefGoogle Scholar
  45. Vedder O, Magrath MJL, Harts AMF, Schut E, van der Velde M, Komdeur J (2010) Reduced extrapair paternity in response to experimental stimulation of earlier incubation onset in blue tits. Behav Ecol 21:9–15CrossRefGoogle Scholar
  46. Venier LA, Robertson RJ (1991) Copulation behaviour of the tree swallow, Tachycineta bicolor: paternity assurance in the presence of sperm competition. Anim Behav 42:939–948CrossRefGoogle Scholar
  47. Wishart GJ (1987) Regulation of the length of the fertile period in the domestic fowl by numbers of oviductal spermatozoa, as reflected by those trapped in laid eggs. J Reprod Fertil 80:493–498PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Arild Johnsen
    • 1
  • Kim L. Carter
    • 2
  • Kaspar Delhey
    • 2
    • 3
  • Jan T. Lifjeld
    • 1
  • Raleigh J. Robertson
    • 4
  • Bart Kempenaers
    • 2
  1. 1.National Centre for Biosystematics, Natural History MuseumUniversity of OsloOsloNorway
  2. 2.Department of Behavioural Ecology and Evolutionary GeneticsMax Planck Institute for OrnithologyStarnberg (Seewiesen)Germany
  3. 3.School of Biological SciencesMonash UniversityClaytonAustralia
  4. 4.Department of BiologyQueen’s UniversityKingstonCanada

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