Skip to main content
Log in

No evidence that sperm morphology predicts paternity success in wild house wrens

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Postcopulatory sexual selection (PCSS) in internally fertilizing vertebrates is a topic of great interest, yet relatively little is known about the characteristics of sperm and ejaculates that confer an advantage in PCSS. In this study, we investigated several measures of sperm morphology that potentially contribute to fertilization success under PCSS. We tested whether sperm morphology related to success in PCSS (via extra-pair paternity) in house wrens (Troglodytes aedon). We found no evidence that sperm morphology differed between extra-pair sires and the within-pair males they cuckolded, nor that sperm morphology correlated with the proportion of within-pair offspring sired, the number of extra-pair offspring sired, or the total annual reproductive success. Male behavioral strategies may affect the probability that their sperm compete with other males’ sperm and that their sperm succeed under competition. Effects of these behavioral strategies, as well as differences between males in sperm number, could mask the effects of sperm morphology on the outcome of PCSS. Despite moderate levels of extra-pair paternity, selection on sperm may be relatively weak in house wrens. Further work is needed to understand general patterns in how sperm morphology relates to fertilization success within species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302

    Article  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 57:289–300

    Google Scholar 

  • Birkhead TR, Fletcher F (1995) Depletion determines sperm numbers in male zebra finches. Anim Behav 49:451–456

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic, San Diego

    Google Scholar 

  • Birkhead TR, Atkin L, Møller AP (1987) Copulation behaviour of birds. Behaviour 101:101–138

    Article  Google Scholar 

  • 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 266:1759–1764

    Article  CAS  Google Scholar 

  • Briskie JV, Montgomerie R, Birkhead TR (1997) The evolution of sperm size in birds. Evolution 51:937–945

    Article  Google Scholar 

  • Brylawski AMZ, Whittingham LA (2004) An experimental study of mate guarding and paternity in house wrens. Anim Behav 68:1417–1424

    Article  Google Scholar 

  • Calhim S, Immler S, Birkhead TR (2007) Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One 2:e413

    Article  PubMed  Google Scholar 

  • Calhim S, Double MC, Margraf N, Birkhead TR, Cockburn A (2011) Maintenance of sperm variation in a highly promiscuous wild bird. PLoS One 6:e28809

    Article  PubMed  CAS  Google Scholar 

  • Cohen J (1967) Correlation between sperm “redundancy” and chiasma frequency. Nature 215:862–863

    Article  PubMed  CAS  Google Scholar 

  • Cramer ERA (2013) Physically challenging song traits, male quality, and reproductive success in house wrens. PLoS One 8:e59208

    Article  PubMed  CAS  Google Scholar 

  • Cramer ERA, Laskemoen T, Kleven O, Lifjeld JT (2013) Sperm length variation in house wrens Troglodytes aedon. J Ornithol 154:129–138

    Article  Google Scholar 

  • 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 77:183–187

    Article  Google Scholar 

  • Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93:504–509

    Article  PubMed  CAS  Google Scholar 

  • Delmore KE, Kleven O, Laskemoen T, Crowe SA, Lifjeld JT, Robertson JR (2008) Sex allocation and parental quality in tree swallows. Behav Ecol 19:1243–1249

    Article  Google Scholar 

  • 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 16:825–833

    Article  Google Scholar 

  • Donoghue AM, Sonstegard TS, King LM, Smith EJ, Burt DW (1999) Turkey sperm mobility influences paternity in the context of competitive fertilization. Biol Reprod 61:422–427

    Article  PubMed  CAS  Google Scholar 

  • Dunn PO, Cockburn A (1998) Costs and benefits of extra-group paternity in superb fairy-wrens. Ornithol Monogr 49:147–161

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Firman RC, Simmons LW (2008) Polyandry, sperm competition, and reproductive success in mice. Behav Ecol 19:695–702

    Article  Google Scholar 

  • Forsman AM, Vogel LA, Sakaluk SK, Johnson BG, Masters BS, Johnson LS, Thompson CF (2008) Female house wrens (Troglodytes aedon) increase the size, but not immunocompetence, of their offspring through extra-pair mating. Mol Ecol 17:3697–3706

    Article  PubMed  Google Scholar 

  • Fossøy F, Johnsen A, Lifjeld JT (2006) Evidence of obligate female promiscuity in a socially monogamous passerine. Behav Ecol Sociobiol 60:255–259

    Article  Google Scholar 

  • Gage MJG, Morrow EH (2003) Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr Biol 13:754–757

    Article  PubMed  CAS  Google Scholar 

  • 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 14:44–47

    PubMed  CAS  Google Scholar 

  • García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution 61:816–824

    Article  PubMed  Google Scholar 

  • Gasparini C, Simmons LW, Beveridge M, Evans JP (2010) Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS One 5:e12146

    Article  PubMed  Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    Article  PubMed  CAS  Google Scholar 

  • 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 39:647–652

    Article  Google Scholar 

  • Helfenstein F, Podevin M, Richner H (2010) Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64:557–565

    Article  Google Scholar 

  • Immler S, Birkhead TR (2007) Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proc R Soc Lond B 274:561–568

    Article  Google Scholar 

  • Immler S, Calhim S, Birkhead TR (2008) Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538–1543

    Article  PubMed  Google Scholar 

  • Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Prounounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643

    Article  PubMed  Google Scholar 

  • Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. P Natl Acad Sci USA 108:5325–5330

    Article  CAS  Google Scholar 

  • Johnsen A, Carter KL, Delhey K, Lifjeld JT, Robertson RJ, Kempenaers B (2012) Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories. Behav Ecol Sociobiol 66:181–190

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • 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 62:494–499

    Article  PubMed  Google Scholar 

  • 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 63:2466–2473

    Article  PubMed  Google Scholar 

  • Kleven O, Laskemoen T, Lifjeld JT (2009b) Sperm length in sand martins Riparia riparia: a comment on Helfenstein et al. J Avian Biol 40:241–242

    Article  Google Scholar 

  • Knudsen J (2009) Sperm production and variance in sperm quality. Master’s thesis, Queen’s University

  • Kvarnemo C, Simmons LW (2013) Polyandry as a mediator of sexual selection before and after mating. Philos T Roy Soc B 368:20120042

    Article  Google Scholar 

  • LaBarbera K, Llambías PE, Cramer ERA, Schaming TD, Lovette IJ (2010) Synchrony does not explain extrapair paternity rate variation in northern or southern house wrens. Behav Ecol 21:773–780

    Article  Google Scholar 

  • Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, Lifjeld JT (2010) Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor. Behav Ecol Sociobiol 64:1473–1483

    Article  Google Scholar 

  • Lifjeld JT, Laskemoen T, Kleven O, Albrecht T, Robertson RJ (2010) Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS One 5:e13456

    Article  PubMed  Google Scholar 

  • Lifjeld JT, Laskemoen T, Kleven O, Pedersen ATM, Lampe HM, Rudolfsen G, Schmoll T, Slagsvold T (2012) No evidence for pre-copulatory sexual selection on sperm length in a passerine bird. PLoS One 7:e32611

    Article  PubMed  CAS  Google Scholar 

  • Liljedal S, Rudolfsen G, Folstad I (2008) Factors predicting male fertilization success in an external fertilizer. Behav Ecol Sociobiol 62:1805–1811

    Article  Google Scholar 

  • Llambías PE, LaBarbera K, Astié AA (2012) Similar patterns of parental provisioning in a monogamous and a polygynous population of the house wren. Condor 114:629–638

    Article  Google Scholar 

  • Lüpold S, Calhim S, Immler S, Birkhead TR (2009a) Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276:1175–1181

    Article  Google Scholar 

  • Lüpold S, Linz GM, Birkhead TR (2009b) Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63:899–909

    Article  Google Scholar 

  • Lüpold S, Manier MK, Berben KS, Smith KJ, Daley BD, Buckley SH, Belote JM, Pitnick S (2012) How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 22:1667–1672

    Article  PubMed  Google Scholar 

  • Michl G, Török J, Griffith SC, Sheldon BC (2002) Experimental analysis of sperm competition mechanisms in a wild bird population. P Natl Acad Sci USA 99:5466–5470

    Article  CAS  Google Scholar 

  • Møller AP, Briskie JV (1995) Extra-pair paternity, sperm competition and the evolution of testis size in birds. Behav Ecol Sociobiol 36:357–365

    Article  Google Scholar 

  • Mossman J, Slate J, Humphries S, Birkhead T (2009) Sperm morphology and velocity are genetically codetermined in the zebra finch. Evolution 63:2730–2737

    Article  PubMed  Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

    Article  Google Scholar 

  • Pattarini JM, Starmer WT, Bjork A, Pitnick S (2006) Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60:2064–2080

    PubMed  Google Scholar 

  • Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, Amsterdam, pp 207–245

    Chapter  Google Scholar 

  • Pizzari T, Cornwallis CK, Lovlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. Available: www.R-project.org

  • Read AF, Weary DM (1992) The evolution of bird song: comparative analyses. Philos T Roy Soc B 338:165–187

    Article  Google Scholar 

  • Rowe M, Pruett-Jones S (2011) Sperm competition selects for sperm quantity and quality in the Australian Maluridae. PLoS One 6:e15720

    Article  PubMed  CAS  Google Scholar 

  • Rudolfsen G, Figenschou L, Folstad I, Kleven O (2008) Sperm velocity influence paternity in the Atlantic cod (Gadus morhua L.). Aquacult Res 39:212–216

    Article  Google Scholar 

  • Sheldon BC (1994) Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257:25–30

    Article  Google Scholar 

  • Simmons LW, Fitzpatrick JL (2012) Sperm wars and the evolution of male fertility. Reproduction 144:519–534

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW, Wernham J, García-González F, Kamien D (2003) Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length. Behav Ecol 14:539–545

    Article  Google Scholar 

  • Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20:46–53

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Paula Cohen and Bob Doran for access to their microscope; Dan Fergus, Kelly Zamudio, Sigal Balshine, Kern Reeve, Wes Hochachka, Jon Lambert, Emma Greig, Melissah Rowe, Arild Johnsen, the NBB Behavior reading group, and the Webster and Lovette labs for thought-provoking discussions; and two anonymous reviewers for comments that improved the manuscript. Paulo Llambías and Taza Schaming initiated the study population. This research was supported by a National Science Foundation Graduate Research Fellowship, the Nordic Research Opportunity Fellowship, and grants from the American Ornithologists’ Union, Animal Behavior Society, Cornell University Department of Neurobiology and Behavior, and Cornell Lab of Ornithology to ERAC, and an Einhorn Discovery Grant to KL. This manuscript was part of ERAC’s PhD dissertation, completed at Cornell University.

Ethical standards

This study complied with the current laws of the countries in which it was performed. Animal use was approved under Cornell Institutional Animal Care and Use Committee (Protocol 2007–0123), and the appropriate state and federal bird banding permits were obtained (numbers 1231 and 20954, respectively).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emily R. A. Cramer.

Additional information

Communicated by D. Rubenstein

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 242 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cramer, E.R.A., Laskemoen, T., Kleven, O. et al. No evidence that sperm morphology predicts paternity success in wild house wrens. Behav Ecol Sociobiol 67, 1845–1853 (2013). https://doi.org/10.1007/s00265-013-1594-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1594-6

Keywords

Navigation