Advertisement

Behavioral Ecology and Sociobiology

, Volume 64, Issue 9, pp 1473–1483 | Cite as

Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor

  • Terje Laskemoen
  • Oddmund Kleven
  • Frode Fossøy
  • Raleigh J. Robertson
  • Geir Rudolfsen
  • Jan T. Lifjeld
Original Paper

Abstract

Sperm competition is widespread among animal taxa and considered a major force in sperm evolution. Recent comparative studies have indicated that sperm competition selects for high sperm production capacity and long and fast-swimming spermatozoa across species. Here, we examine the role of sperm quantity and quality for fertilization success of individual males in a Canadian population of tree swallows Tachycineta bicolor, a socially monogamous, but highly promiscuous passerine. Male fertilization success (the sum of withinpair and extrapair young) was significantly associated with the size of the cloacal protuberance (a proxy for sperm quantity), but not with sperm size or in vitro sperm swimming speed. In a multivariate analysis, both cloacal protuberance volume and relative sperm midpiece size (i.e. high mitochondrial loading) had significant effects on male fertilization success. However, relative sperm midpiece size was not associated with fertilization success in a simple regression. Further, both cloacal protuberance volume and relative midpiece size had significant effects on sperm velocity, both in simple regressions and in a multivariate analysis. The finding that males with large relative midpiece size had both higher fertilization success and faster swimming sperm, suggests an indirect link between sperm morphology and male fertility mediated through sperm velocity. In conclusion, both quantitative and qualitative sperm traits seem to affect male fertilization success in tree swallows.

Keywords

Cloacal protuberance Sperm competition Sperm length Sperm motility Tachycineta bicolor Tree swallow 

Notes

Acknowledgements

We are grateful to Susan A. Crowe, Kira E. Delmore and Hannah Munro for assistance with field work, and the staff at the Queen's University Biological Station for logistical support. Two anonymous referees are thanked for valuable comments on an earlier draft of the manuscript. This study was funded by grants from the Natural Sciences and Engineering Research Council of Canada (grant no. RGPIN/6691-2006) to R.J.R. and the Research Council of Norway (grant no. 170853/V40) to J.T.L. Sampling for this study was conducted under Queen’s University Animal Care permit 2005-021-R1, Canadian Wildlife Service (CWS) banding permit 10302, and CWS scientific capture permit CA0156.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Birkhead TR, Møller AP (1998) Sperm competition, sexual selection and different routes to fitness. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 757–781CrossRefGoogle Scholar
  2. Birkhead TR, Pizzari T (2002) Post-copulatory sexual selection. Nat Rev Genet 3:262–273CrossRefPubMedGoogle Scholar
  3. Birkhead TR, Briskie JV, Møller AP (1993) Male sperm reserves and copulation frequency in birds. Behav Ecol Sociobiol 32:85–93CrossRefGoogle Scholar
  4. Birkhead TR, Buchanan KL, Devoogd TJ, Pellatt EJ, Szekely T, Catchpole CK (1997) Song, sperm quality and testes asymmetry in the sedge warbler. Anim Behav 53:965–971CrossRefGoogle Scholar
  5. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc B 266:1759–1764CrossRefPubMedGoogle Scholar
  6. Bitton P-P, O'Brien EL, Dawson RD (2007) Plumage brightness and age predict extrapair fertilization success of male tree swallows, Tachycineta bicolor. Anim Behav 74:1777–1784CrossRefGoogle Scholar
  7. Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc R Soc B 247:89–95CrossRefPubMedGoogle Scholar
  8. Briskie JV, Montgomerie R, Birkhead TR (1997) The evolution of sperm size in birds. Evolution 51:937–945CrossRefGoogle Scholar
  9. Calhim S, Immler S, Birkhead TR (2007) Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2:e413CrossRefPubMedGoogle Scholar
  10. Cardullo RA, Baltz JM (1991) Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency. Cell Motil Cytoskelet 19:180–188CrossRefGoogle Scholar
  11. Casselman SJ, Schulte-Hostedde AI, Montgomerie R (2006) Sperm quality influences fertilization success in the walleye (Sander vitreus). Can J Fish Aquat Sci 63:2119–2125CrossRefGoogle Scholar
  12. Crowe SA, Kleven O, Delmore KE, Laskemoen T, Nocera JJ, Lifjeld JT, Robertson JR (2009) Paternity assurance through frequent copulations in a wild passerine with intense sperm competition. Anim Behav 77:183–187CrossRefGoogle Scholar
  13. Delmore KE, Kleven O, Laskemoen T, Crowe SA, Lifield JT, Robertson JR (2008) Sex allocation and parental quality in tree swallows. Behav Ecol 19:1243–1249CrossRefGoogle Scholar
  14. Denk AG, Kempenaers B (2006) Testosterone and testes size in mallards (Anas platyrhynchos). J Ornithol 147:436–440CrossRefGoogle Scholar
  15. 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
  16. Deviche P, Wingfield JC, Sharp PJ (2000) Year-class differences in the reproductive system, plasma prolactin and corticosterone concentrations, and onset of prebasic molt in male dark-eyed juncos (Junco hyemalis) during the breeding period. Gen Comp Endocrinol 118:425–435CrossRefPubMedGoogle Scholar
  17. Dickinson JL (2001) Extrapair copulations in western bluebirds (Sialia mexicana): female receptivity favors older males. Behav Ecol Sociobiol 50:423–429CrossRefGoogle Scholar
  18. Donoghue AM, Sonstegard TS, King LM, Smith EJ, Burt DW (1999) Turkey sperm mobility influences paternity in the context of competitive fertilization. Biol Reprod 61:422–427CrossRefPubMedGoogle Scholar
  19. Dunn PO, Cockburn A (1999) Extrapair mate choice and honest signaling in cooperatively breeding superb fairy-wrens. Evolution 53:938–946CrossRefGoogle Scholar
  20. Dunn PO, Whittingham LA, Pitcher TE (2001) Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55:161–175PubMedGoogle Scholar
  21. Dunn PO, Lifjeld JT, Whittingham LA (2009) Multiple paternity and offspring quality in tree swallows. Behav Ecol Sociobiol 63:911–922CrossRefGoogle Scholar
  22. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  23. Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals—an unpaved road to the egg. Nat Rev Mol Cell Biol 7:276–285CrossRefPubMedGoogle Scholar
  24. Evans MR, Goldsmith AR (2000) Male wrens with large testes breed early. Anim Behav 60:101–105CrossRefPubMedGoogle Scholar
  25. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci USA 106:1128–1132CrossRefPubMedGoogle Scholar
  26. Gage MJG (1998) Mammalian sperm morphometry. Proc R Soc B 265:97–103CrossRefPubMedGoogle Scholar
  27. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47PubMedGoogle Scholar
  28. Garamszegi LZ, Eens M, Hurtrez-Boussès S, Møller AP (2005) Testosterone, testes size, and mating success in birds: a comparative study. Horm Behav 47:389–409CrossRefPubMedGoogle Scholar
  29. Gomendio M, Roldan ERS (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52:439–447CrossRefPubMedGoogle Scholar
  30. Graves GR (2004) Testicular volume and asymmetry are age-dependent in black-throated blue warblers (Dendroica caerulescens). Auk 121:473–485CrossRefGoogle Scholar
  31. Helfenstein F, Szép T, Nagy Z, Kempenaers B, Wagner RH (2008) Between-male variation in sperm size, velocity and longevity in sand martins Riparia riparia. J Avian Biol 39:649–652CrossRefGoogle Scholar
  32. Helfenstein F, Podevin M, Richner H (2010) Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64:557–565CrossRefGoogle Scholar
  33. Hilton FK (1968) Endocrine control of seminal-glomus growth and function in starlings of different ages. Physiol Zool 41:364–370Google Scholar
  34. Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319Google Scholar
  35. Immler S, Birkhead TR (2007) Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proc R Soc B 274:561–568CrossRefPubMedGoogle Scholar
  36. Immler S, Saint-Jalme M, Lesobre L, Sorci G, Roman Y, Birkhead TR (2007) The evolution of sperm morphometry in pheasants. J Evol Biol 20:1008–1014CrossRefPubMedGoogle Scholar
  37. Immler S, Calhim S, Birkhead TR (2008) Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538–1543CrossRefPubMedGoogle Scholar
  38. Johnsen A, Lifjeld JT, Andersson S, Örnborg J, Amundsen T (2001) Male characteristics and fertilisation success in bluethroats. Behaviour 138:1371–1390CrossRefGoogle Scholar
  39. Kempenaers B, Everding S, Bishop C, Boag P, Robertson RJ (2001) Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor). Behav Ecol Sociobiol 49:251–259CrossRefGoogle Scholar
  40. Kempenaers B, Peer K, Vermeirssen ELM, Robertson RJ (2002) Testes size and asymmetry in the tree swallow Tachycineta bicolor: a test of the compensation hypothesis. Avian Sci 2:115–122Google Scholar
  41. Kleven O, Marthinsen G, Lifjeld JT (2006) Male extraterritorial forays, age and paternity in the socially monogamous reed bunting (Emberiza schoeniclus). J Ornithol 147:468–473CrossRefGoogle Scholar
  42. Kleven O, Laskemoen T, Fossøy F, Robertson RJ, Lifjeld JT (2008) Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62:494–499CrossRefPubMedGoogle Scholar
  43. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT (2009a) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63:2466–2473CrossRefPubMedGoogle Scholar
  44. Kleven O, Laskemoen T, Lifjeld JT (2009b) Sperm length in sand martins: a comment on Helfenstein et al. J Avian Biol 40:241–242CrossRefGoogle Scholar
  45. Koehler LD (1995) Diversity of avian spermatozoa ultrastructure with emphasis on the members of the order Passeriformes. Mém Mus Natn Hist Nat 166:437–444Google Scholar
  46. Laskemoen T, Kleven O, Fossøy F, Lifjeld JT (2007) Intraspecific variation in sperm length in two passerine species, the bluethroat Luscinia svecica and the willow warbler Phylloscopus trochilus. Ornis Fenn 84:131–139Google Scholar
  47. Laskemoen T, Fossøy F, Rudolfsen G, Lifjeld JT (2008) Age-related variation in primary sexual characters in a passerine with male age-related fertilization success, the bluethroat Luscinia svecica. J Avian Biol 39:322–328CrossRefGoogle Scholar
  48. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  49. Levitan DR (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proc R Soc B 267:531–534CrossRefPubMedGoogle Scholar
  50. Lifjeld JT, Robertson RJ (1992) Female control of extra-pair fertilization in tree swallows. Behav Ecol Sociobiol 31:89–96CrossRefGoogle Scholar
  51. Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45:213–229CrossRefGoogle Scholar
  52. Lüpold S, Calhim S, Immler S, Birkhead TR (2009a) Sperm morphology and sperm velocity in passerine birds. Proc R Soc B 276:1175–1181CrossRefPubMedGoogle Scholar
  53. Lüpold S, Linz GM, Birkhead TR (2009b) Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63:899–909CrossRefGoogle Scholar
  54. Malo AF, Garde JJ, Soler AJ, Garcia AJ, Gomendio M, Roldan ERS (2005) Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 72:822–829CrossRefPubMedGoogle Scholar
  55. Malo AF, Roldan ERS, Garde JJ, Soler AJ, Vicente J, Gortazar C, Gomendio M (2009) What does testosterone do for red deer males? Proc R Soc B 276:971–980CrossRefPubMedGoogle Scholar
  56. Merilä J, Sheldon BC (1999) Testis size variation in the greenfinch Carduelis chloris: relevance for some recent models of sexual selection. Behav Ecol Sociobiol 45:115–123CrossRefGoogle Scholar
  57. Møller AP, Briskie JV (1995) Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav Ecol Sociobiol 36:357–365CrossRefGoogle Scholar
  58. Morrow EH, Gage MJG (2001) Consistent significant variation between individual males in spermatozoal morphometry. J Zool Lond 254:147–153CrossRefGoogle Scholar
  59. Mossman J, Slate J, Humphries S, Birkhead TR (2009) Sperm morphology and velocity are genetically codetermined in the zebra finch. Evolution 63:2730–2737CrossRefPubMedGoogle Scholar
  60. Parker GA (1970) Sperm competition and its evolutionary consequences in insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  61. Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc B 253:245–254CrossRefPubMedGoogle Scholar
  62. Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, San Diego, pp 3–54CrossRefGoogle Scholar
  63. Peer K, Robertson RJ, Kempenaers B (2000) Reproductive anatomy and indices of quality in male tree swallows: the potential reproductive role of floaters. Auk 117:74–81CrossRefGoogle Scholar
  64. Penfold LM, Wildt DE, Herzog TL, Lynch W, Ware L, Derrickson SE, Monfort SL (2000) Seasonal patterns of LH, testosterone and semen quality in the Northern pintail duck (Anas acuta). Reprod Fertil Dev 12:229–235CrossRefPubMedGoogle Scholar
  65. Pitcher TE, Dunn PO, Whittingham LA (2005) Sperm competition and the evolution of testes size in birds. J Evol Biol 18:557–567CrossRefPubMedGoogle Scholar
  66. Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, San Diego, pp 207–245Google Scholar
  67. Richardson DS, Burke T (1999) Extra-pair paternity in relation to male age in Bullock's orioles. Mol Ecol 8:2115–2126CrossRefPubMedGoogle Scholar
  68. Robertson RJ, Rendell WB (2001) A long-term study of reproductive performance in tree swallows: the influence of age and senescence on output. J Anim Ecol 70:1014–1031CrossRefGoogle Scholar
  69. Rowe M, Pruett-Jones S (2006) Reproductive biology and sperm competition in Australian fairy-wrens. Avian Poult Biol Rev 17:21–37CrossRefGoogle Scholar
  70. Rudolfsen G, Figenschou L, Folstad I, Kleven O (2008) Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.). Aquac Res 39:212–216Google Scholar
  71. Schmoll T, Mund V, Dietrich-Bischoff V, Winkel W, Lubjuhn T (2007) Male age predicts extrapiar and total fertilization success in the socially monogamous coal tit. Behav Ecol 18:1073–1081CrossRefGoogle Scholar
  72. Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53CrossRefPubMedGoogle Scholar
  73. Stapleton MK, Kleven O, Lifield JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 161:1725–1733CrossRefGoogle Scholar
  74. Stockley P (1997) Sexual conflict resulting from adaptations to sperm competition. Trends Ecol Evol 12:154–159CrossRefGoogle Scholar
  75. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027CrossRefPubMedGoogle Scholar
  76. Tuttle EM, Pruett-Jones S (2004) Estimates of extreme sperm production: morphological and experimental evidence from reproductively promiscuous fairy-wrens (Malurus). Anim Behav 68:541–550CrossRefGoogle Scholar
  77. Tuttle EM, Pruett-Jones S, Webster MS (1996) Cloacal protuberances and extreme sperm production in Australian fairy-wrens. Proc R Soc B 263:1359–1364CrossRefGoogle Scholar
  78. Venier LA, Robertson RJ (1991) Copulation behavior of the tree swallow, Tachycineta bicolor: paternity assurance in the presence of sperm competition. Anim Behav 42:939–948CrossRefGoogle Scholar
  79. Vernon GG, Woolley DM (1999) Three-dimensional motion of avian spermatozoa. Cell Motil Cytoskelet 42:149–161CrossRefGoogle Scholar
  80. Ward PI (1998) Intraspecific variation in sperm size characters. Heredity 80:655–659CrossRefPubMedGoogle Scholar
  81. Weatherhead PJ, Boag PT (1995) Pair and extra-pair mating success relative to male quality in red-winged blackbirds. Behav Ecol Sociobiol 37:81–91CrossRefGoogle Scholar
  82. Wetton JH, Burke T, Parkin DT, Cairns E (1995) Single-locus DNA-fingerprinting reveals that male reproductive success increases with age through extra-pair paternity in the house sparrow (Passer domesticus). Proc R Soc B 260:91–98CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Terje Laskemoen
    • 1
  • Oddmund Kleven
    • 1
    • 2
  • Frode Fossøy
    • 1
    • 3
  • Raleigh J. Robertson
    • 4
  • Geir Rudolfsen
    • 5
  • Jan T. Lifjeld
    • 1
  1. 1.National Centre for Biosystematics, Natural History MuseumUniversity of OsloOsloNorway
  2. 2.Faculty of Biosciences and AquacultureBodø University CollegeBodøNorway
  3. 3.Department of BiologyNorwegian University of Science and TechnologyTrondheimNorway
  4. 4.Department of BiologyQueen’s UniversityKingstonCanada
  5. 5.Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and EconomicsUniversity of TromsøTromsøNorway

Personalised recommendations