Skip to main content
Log in

No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia)

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Genetic parentage studies of socially monogamous birds reveal a widespread prevalence of extra-pair paternity. Variation in extra-pair paternity among individuals may depend on how different individuals benefit from extra-pair fertilisations and on the opportunity to pursue extra-pair copulations. A long-term study of sand martins (Riparia riparia) in Hungary allowed us to examine patterns of extra-pair fertilisations in a large colony of over 3,000 breeding pairs with many known age individuals. We used multi-locus DNA fingerprinting to determine whether extra-pair fertilisations occur when females are paired to (1) presumably low quality mates, or (2) genetically similar or dissimilar mates, and whether extra-pair fertilisations result in offspring of higher quality. Extra-paternal young were found in 38% of 47 broods and comprised 19% of 190 offspring. Males that lost paternity did not differ significantly from others in age or body condition. Social mates of broods containing extra-pair offspring did not differ in genetic similarity from pairs without extra-pair offspring. Furthermore, there was no significant difference in body condition between extra-pair young and their maternal half-siblings. We were unable to assign paternity and therefore cannot exclude the possibility that extra-pair males differed from the within-pair males they cuckolded, in age, body condition or genetic similarity with the female. We found a positive relationship between paternity losses and breeding density, suggesting that low breeding density may constrain opportunities for seeking extra-pair copulations.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alves MAS, Bryant DM (1998) Brood parasitism in the sand martin, Riparia riparia: evidence for two parasitic strategies in a colonial passerine. Anim Behav 56:1323–1331

    CAS  PubMed  Google Scholar 

  • Aviv A (2002) Chronology versus biology—telomeres, essential hypertension, and vascular aging. Hypertension 40:229–232

    CAS  PubMed  Google Scholar 

  • Bateson P (1983) Optimal outbreeding. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 257–277

    Google Scholar 

  • Beecher MD, Beecher IM (1979) Sociobiology of bank swallows—reproductive strategy of the male. Science 205:1282–1285

    CAS  PubMed  Google Scholar 

  • Birkhead TR, Møller AP (1992) Sperm competition in birds. Evolutionary causes and consequences. Academic, London

    Google Scholar 

  • Bjørnstad G, Lifjeld JT (1997) High frequency of extra-pair paternity in a dense and synchronous population of willow warblers Phylloscopus trochilus. J Avian Biol 28:319–324

    Google Scholar 

  • Blomqvist D, Andersson M, Küpper C, Cuthill IC, Kis J, Lanctot RB, Sandercock BK, Székely T, Wallander J, Kempenaers B (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615

    CAS  PubMed  Google Scholar 

  • Bouwman KM, Komdeur J (2005) Old female reed buntings (Emberiza schoeniclus) increase extra-pair paternity in their broods when mated to young males. Behaviour 142:1449–1463

    Google Scholar 

  • Bouwman KM, Burke T, Komdeur J (2006a) How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods. Mol Ecol 15:2589–2600

    CAS  PubMed  Google Scholar 

  • Bouwman KM, Burke T, Komdeur J (2006b) Older male reed buntings are more successful at gaining within- and extra-pair fertilizations. Anim Behav (in press)

  • Brooks R, Kemp DJ (2001) Can older males deliver the good genes? Trends Ecol Evol 16:308–313

    CAS  PubMed  Google Scholar 

  • Charmantier A, Perret P (2004) Manipulation of nest-box density affects extra-pair paternity in a population of blue tits (Parus caeruleus). Behav Ecol Sociobiol 56:360–365

    Google Scholar 

  • Charmantier A, Blondel J, Perret P, Lambrechts MM (2004) Do extra-pair paternities provide genetic benefits for female blue tits Parus caeruleus? J Avian Biol 35:524–532

    Google Scholar 

  • Dietrich V, Schmoll T, Winkel W, Epplen JT, Lubjuhn T (2004) Pair identity—an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141:817–835

    Google Scholar 

  • Eimes JA, Parker PG, Brown JL, Brown ER (2005) Extrapair fertilization and genetic similarity of social mates in the Mexican jay. Behav Ecol 16:456–460

    Google Scholar 

  • Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717

    CAS  PubMed  Google Scholar 

  • Greene E, Lyon BE, Muehter VR, Ratcliffe L, Oliver SJ, Boag PT (2000) Disruptive sexual selection for plumage coloration in a passerine bird. Nature 407:1000–1003

    CAS  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

    CAS  PubMed  Google Scholar 

  • Haffer J (1985) Riparia. In: Glutz von Blotzheim UN, Bauer MB (eds) Handbuch der Vögel Mitteleuropas - Passeriformes (1.Teil). AULA, Wiesbaden, pp 315–366

    Google Scholar 

  • Hansson B, Bensch S, Hasselquist D, Akesson M (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc R Soc Lond B 268:1287–1291

    CAS  Google Scholar 

  • Hasselquist D, Bensch S, vonSchantz T (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381:229–232

    CAS  Google Scholar 

  • Haussmann MF, Winkler DW, Vleck CM (2005) Longer telomeres associated with higher survival in birds. Biol Lett 1:212–214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoi H, Hoi-Leitner M (1997) An alternative route to coloniality in the bearded tit: females pursue extra-pair fertilizations. Behav Ecol 8:113–119

    Google Scholar 

  • Johnsen A, Lifjeld JT, Andersson S, Ornborg J, Amundsen T (2001) Male characteristics and fertilisation success in bluethroats. Behaviour 138:1371–1390

    Google Scholar 

  • Kania W (2001) Age determination of the great tit Parus major nestlings by means of the probability method based on feather development. Notatki Ornitol 42:117–138

    Google Scholar 

  • Kempenaers B, Verheyren GR, Dhondt AA (1997) Extrapair paternity in the blue tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492

    Google Scholar 

  • Kleven O, Marthinsen G, Lifjeld JT (2006) Male extraterritorial forays, age and paternity in the socially monogamous reed bunting (Emberiza schoeniclus). J Ornithol 147:468–473

    Google Scholar 

  • Kokko H (2001) Fisherian and “good genes” benefits of mate choice: how (not) to distinguish between them. Ecol Lett 4:322–326

    Google Scholar 

  • Kokko H, Lindström J (1996) Evolution of female preference for old mates. Proc R Soc Lond B 263:1533–1538

    Google Scholar 

  • Kokko H, Ots I (2006) When not to avoid inbreeding. Evolution 60:467–475

    PubMed  Google Scholar 

  • Krokene C, Anthonisen K, Lifjeld JT, Amundsen T (1996) Paternity and paternity assurance behaviour in the bluethroat, Luscinia s. svecica.Anim Behav 52:405–417

    Google Scholar 

  • Manning JT (1985) Choosy females and correlates of male age. J Theor Biol 116:349–354

    Google Scholar 

  • Marshall RC, Buchanan KL, Catchpole CK (2003) Sexual selection and individual genetic diversity in a songbird. Proc R Soc Lond B 270:S248–S250

    Google Scholar 

  • Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559

    PubMed  Google Scholar 

  • Møller AP, Brohede J, Cuervo JJ, de Lope F, Primmer C (2003) Extrapair paternity in relation to sexual ornamentation, arrival date, and condition in a migratory bird. Behav Ecol 14:707–712

    Google Scholar 

  • Morton ES, Forman L, Braun M (1990) Extrapair fertilizations and the evolution of colonial breeding in purple martins. Auk 107:275–283

    Google Scholar 

  • Pauliny A, Wagner RH, Augustin J, Szep T, Blomqvist D (2006) Age-independent telomere length predicts fitness in two bird species. Mol Ecol 15:1681–1687

    CAS  PubMed  Google Scholar 

  • Perry JN, Liebhold AM, Rosenberg MS, Dungan J, Miriti M, Jakomulska A, Citron-Pousty S (2002) Illustrations and guidelines for selecting statistical methods for quantifying spatial pattern in ecological data. Ecography 25:578–600

    Google Scholar 

  • Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58

    CAS  PubMed  Google Scholar 

  • Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206

    CAS  PubMed  Google Scholar 

  • Rätti O, Hovi M, Lundberg A, Tegelström H, Alatalo RV (1995) Extra-pair paternity and male characteristics in the pied flycatcher. Behav Ecol Sociobiol 37:419–425

    Google Scholar 

  • Richardson DS, Burke T (1999) Extra-pair paternity in relation to male age in Bullock’s orioles. Mol Ecol 8:2115–2126

    CAS  PubMed  Google Scholar 

  • Seddon N, Amos W, Mulder RA, Tobias JA (2004) Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird. Proc R Soc Lond B 271:1823–1829

    Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    CAS  Google Scholar 

  • Sheldon BC, Merilä J, Qvarnström A, Gustafsson L, Ellegren H (1997) Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264:297–302

    Google Scholar 

  • Shin HS, Bargiello TA, Clark BT, Jackson FR, Young MW (1985) An unusual coding sequence from a Drosophila clock gene is conserved in vertebrates. Nature 317:445–448

    CAS  PubMed  Google Scholar 

  • Siegel S, Castellan NJJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Slagsvold T, Lifjeld JT (1997) Incomplete female knowledge of male quality may explain variation in extra-pair paternity in birds. Behaviour 134:353–371

    Google Scholar 

  • Stutchbury BJM (1998) Female mate choice of extra-pair males: breeding synchrony is important. Behav Ecol Sociobiol 43:213–215

    Google Scholar 

  • Sundberg J, Dixon A (1996) Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim Behav 52:113–122

    Google Scholar 

  • Svensson S (1969) Häckningsbiologiska studier i en koloni av backsvala, Riparia riparia,vid Ammarnäs år 1968. Fagelvarld 8:236–240

    Google Scholar 

  • Szép T (1992) Nine year old sand martin (Riparia riparia) recovery in Eastern Hungary. Aquila 99:189

    Google Scholar 

  • Szép T (1999) Effects of age- and sex-biased dispersal on the estimation of survival rates of the sand martin Riparia riparia population in Hungary. Bird Study 46:169–177

    Google Scholar 

  • Szép T, Møller AP (1999) Cost of parasitism and host immune defence in the sand martin Riparia riparia: a role for parent–offspring conflict? Oecologia 119:9–15

    PubMed  Google Scholar 

  • Szép T, Szabó ZD, Vallner J (2003) Integrated population monitoring of sand martin Riparia riparia—an opportunity to monitor the effects of environmental disasters along the river Tisza. Ornis Hung 12–13:169–182

    Google Scholar 

  • Tarof SA, Ratcliffe LM, Kasumovic MM, Boag PT (2005) Are least flycatcher (Empidonax minimus) clusters hidden leks? Behav Ecol 16:207–217

    Google Scholar 

  • Tarvin KA, Webster MS, Tuttle EM, Pruett-Jones S (2005) Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens. Anim Behav 70:945–955

    Google Scholar 

  • Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027

    CAS  PubMed  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selction. In: Campbell B (eds) Sexual selection and the descent of man: 1871–1971. Aldine, Chicago, pp 136–179

    Google Scholar 

  • Wagner RH (1993) The pursuit of extra-pair copulations by female birds—a new hypothesis of colony formation. J Theor Biol 163:333–346

    Google Scholar 

  • Wagner RH, Schug MD, Morton ES (1996) Confidence of paternity, actual paternity and parental effort by purple martins. Anim Behav 52:123–132

    Google Scholar 

  • Westneat DF (1992) Do female red-winged blackbirds engage in a mixed mating strategy. Ethology 92:7–28

    Google Scholar 

  • Westneat DF (1993) Polygyny and extrapair fertilizations in Eastern red-winged blackbirds (Agelaius–Phoeniceus). Behav Ecol 4:49–60

    Google Scholar 

  • Westneat DF, Sherman PW (1997) Density and extra-pair fertilizations in birds: a comparative analysis. Behav Ecol Sociobiol 41:205–215

    Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Syst 34:365–396

    Google Scholar 

  • Wetton JH, Carter RE, Parkin DT, Walters D (1987) Demographic-study of a wild house sparrow population by DNA fingerprinting. Nature 327:147–149

    CAS  PubMed  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711–1717

    Google Scholar 

  • Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69–75

    Google Scholar 

Download references

Acknowledgments

We thank Jan Lifjeld, Johan Wallander, Erwin Nemeth and two anonymous referees for constructive comments on the manuscript. Tibor Szép was supported by OTKA Grants T29853 and T42879. We also thank the Nyíregyháza Chapter of the MME/BirdLife Hungary for providing tools for the field work, and Noémi Szállassy, Béla Habarics and volunteers of the MME/BirdLife Hungary for assistance in the survey and ringing work. Finally, a very big thank you to Gaute Grønstøl for fruitful discussions and help with the manuscript. Collection of blood samples adhered to the national legal requirements for research with animals (permit number: Hungary, HNP/1873-2/2002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jakob Augustin.

Additional information

Communicated by M. Wink.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Augustin, J., Blomqvist, D., Szép, T. et al. No evidence of genetic benefits from extra-pair fertilisations in female sand martins (Riparia riparia). J Ornithol 148, 189–198 (2007). https://doi.org/10.1007/s10336-006-0119-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-006-0119-8

Keywords