Skip to main content
Log in

Same-sex pair-bonds are equivalent to male–female bonds in a life-long socially monogamous songbird

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

Abstract

Same-sex sexual behaviors are well documented in both captive and wild animals. In monogamous species, these behaviors are often exclusive, each individual having only one same-sex partner. A bias in sex ratio has been proposed as a social context yielding same-sex pair-bonding, but this hypothesis has rarely been tested. Focusing on a life-long pair-bonding songbird, the zebra finch Taeniopygia guttata, we tested whether same-sex pairing results from a shortage of individuals of the opposite sex. By experimentally skewing the sex ratio towards members of one sex, we observed a greater proportion of same-sex pair-bonds of that sex. Moreover, we assessed whether the quality and stability of social interactions were equivalent in same-sex and male–female pairs. Male–male and female–female same-sex bonds display the same behavioral characteristics as male–female ones: they are intense, highly selective, and stable affinitive relationships involving the same behavioral displays already described in wild birds. Moreover, same-sex male bonds were sufficiently strong not to split up when individuals were given the opportunity to reproduce with females. Because the pair-bond in socially monogamous species represents a partnership that may give advantages for survival (e.g., resources defense, fighting against predators, etc.), we propose that same-sex pairing in the zebra finch may result from the pressure to find a social partner.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AP:

Allopreening bouts

CB:

Events of clumping and greeting beak fence

CC:

Courtship and copulation

DS:

Directed songs

I RS :

Index of relationship strength

I RSd :

Daily value of I RS

I RStot :

Value of I RS computed over the whole experiment

NS:

Nest sharing

OV:

Outcome variable

References

  • Adkins-Regan E (2002) Development of sexual partner preference in the zebra finch: a socially monogamous, pair-bonding animal. Arch Sex Behav 31(1):27–33

    Article  PubMed  Google Scholar 

  • Adkins-Regan E (2009) Hormones and sexual differenciation of avian social behavior. Dev Neurosci 31(4):342–350

    Article  PubMed  CAS  Google Scholar 

  • Adkins-Regan E (2011) Neuroendocrine contributions to sexual partner preference in birds. Front Neuroendocrinol 32(2):155–163

    Article  PubMed  CAS  Google Scholar 

  • Adkins-Regan E, Krakauer A (2000) Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch. Anim Behav 60(1):47–53

    Article  PubMed  Google Scholar 

  • Bagemihl B (1999) Biological exuberance: animal homosexuality and natural diversity. Bagemihl, Bruce edn. St. Martin’s Press, NewYork

  • Bailey NW, Zuk M (2009) Same-sex sexual behaviour and evolution. Trends Ecol Evol 24(8):439–446

    Article  PubMed  Google Scholar 

  • Black JM (1996) Pair bonds and partnerships. In: Black JM (ed) Partnerships in birds. The study of monogamy. Oxford University Press, New York, pp 3–20

    Google Scholar 

  • Butterfield PA (1970) The pair bond in the zebra finch. In: Crook JH (ed) Social behaviour in birds and mammals. Academic Press, London, pp 249–278

    Google Scholar 

  • Butts CT, Handcock MS, Hunter DR (2008) Network: classes for relational data. R package version 1.4-1. Irvine, CA

  • Clayton NS (1990) Mate choice and pair formation in timor and australian mainland zebra finches. Anim Behav 39(3):474–480

    Article  Google Scholar 

  • Conover MR, Hunt GL Jr (1984a) Experimental evidence that female–female pairs in gulls result from a shortage of breeding males. Condor 86:472–476

    Article  Google Scholar 

  • Conover MR, Hunt GL Jr (1984b) Female–female pairing and sex ratios in gulls: an historical perspective. Wilson Bull 96:619–625

    Google Scholar 

  • Elie JE, Mariette MM, Soula HA, Griffith SC, Mathevon N, Vignal C (2010) Vocal communication at nest between mates in wild zebra finches: a private vocal duet. Anim Behav 80:597–605

    Article  Google Scholar 

  • Gavrilets S, Rice WR (2006) Genetic models of homosexuality: generating testable predictions. Proc Royal Soc B 273:3031–3038

    Article  Google Scholar 

  • Griffith SC, Holleley CE, Mariette MM, Pryke SR, Svedin N (2010) Low level of extrapair parentage in wild zebra finches. Anim Behav 79:251–254

    Article  Google Scholar 

  • Hall ML (2004) A review of hypotheses for the functions of avian duetting. Behav Ecol Sociobiol 55:415–430

    Article  Google Scholar 

  • Hunt GL Jr, Hunt MW (1977) Female–female pairing in western gulls (Larus occidentalis) in Southern California. Science 196:1466–1467

    Article  PubMed  Google Scholar 

  • Hunt GL Jr, Wingfield JC, Newman A, Farner DS (1980) Sex ratio of western gulls on Santa Barbara Island, California. Auk 97:473–479

    Google Scholar 

  • King CE (2006) Pink flamingos: atypical partnerships and sexual activity in colonially breeding birds. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals. An evolutionary perspective. Cambridge University Press, New York, pp 77–106

    Google Scholar 

  • Kotrschal K, Hemetsberger J, Weiss BM (2006) Making the best of a bad situation: homosociality in male greylag geese. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals. An evolutionary perspective. Cambridge University Press, New York, pp 45–76

    Google Scholar 

  • Kudo H, Dunbar RIM (2001) Neocortex size and social network size in primates. Anim Behav 61:1–11

    Article  Google Scholar 

  • MacFarlane GR, Blomberg SP, Kaplan G, Rogers LJ (2007) Same-sex sexual behavior in birds: expression is related to social mating system and state of development at hatching. Behav Ecol 18:21–33

    Article  Google Scholar 

  • MacFarlane GR, Blomberg SP, Vasey PL (2010) Homosexual behaviour in birds: frequency of expression is related to parental care disparity between the sexes. Anim Behav 80:375–390

    Article  Google Scholar 

  • McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in african elephants. Anim Behav 59:1103–1109

    Article  PubMed  Google Scholar 

  • McGraw KJ, Hill GE (1999) Induced homosexual behaviour in male house finches (Carpodacus mexicanus): the “Prisoner effect”. Ethol Ecol Evol 11:197–201

    Article  Google Scholar 

  • Morris D (1954) The reproductive behavior of the zebra finch (Poephila guttata) with special reference to pseudofemale behaviour and displacement activities. Behaviour 7:1–31

    Article  Google Scholar 

  • Pincemy G, Dobson FS, Jouventin P (2010) Homosexual mating displays in penguins. Ethology 116:1210–1216

    Article  Google Scholar 

  • Poiani A (2010) Animal homosexuality: a biosocial perspective. Cambridge University Press, New York

    Google Scholar 

  • R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reichard UH, Boesch C (2003) Monogamy. Mating strategies and partnerships in birds, humans and other mammals. Cambridge University Press, New York

    Google Scholar 

  • Roselli CE, Stormshak F (2009) Prenatal programming of sexual partner preference: the ram model. J Neuroendocrinol 21(4):359–364

    Article  PubMed  CAS  Google Scholar 

  • Sommer V, Vasey PL (2006) Homosexual behaviour in animals. An evolutionary perspective. Cambridge University Press, New York

    Google Scholar 

  • Van Gossum H, De Bruyn L, Stoks R (2005) Reversible switches between male–male and male–female mating behaviour by male damselflies. Biol Lett 1:268–270

    Article  PubMed  Google Scholar 

  • van Schaik CP, Aureli F (2000) The natural history of valuable relationships in primates. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 307–333

    Google Scholar 

  • Vasey PL, Sommer V (2006) Homosexual behaviour in animals: topics, hypotheses and research trajectories. In: Sommer V, Vasey PL (eds) Homosexual behaviour in animals. An evolutionary perspective. Cambridge University Press, New York, pp 3–42

    Google Scholar 

  • Villella A, Hall JC (2008) Neurogenetics of courtship and mating in Drosophila. Adv Genet 62:67–184

    Article  PubMed  CAS  Google Scholar 

  • Whitehead H, Dufault S (1999) Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. Adv Stud Anim Behav 28:33–74

    Article  Google Scholar 

  • Young LC, Zaun BJ, VanderWerf EA (2010) Successful same-sex pairing in laysan albatross. Biol Lett 4:323–325

    Article  Google Scholar 

  • Zann R, Runciman D (1994) Survivorship, dispersal and sex ratios of zebra finches Taeniopygia guttata in Southeast Australia. Ibis 136:136–146

    Article  Google Scholar 

  • Zann R, Runciman D (2003) Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations. Behav Ecol Sociobiol 54:294–302

    Article  Google Scholar 

  • Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, Oxford

    Google Scholar 

  • Zuk M (2006) Family values in black and white. Nature 439:917

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The authors warmly thank Colette Bouchut and Nicolas Boyer for all the technical support in the ENES laboratory. We are also grateful to Hédi A. Soula for help with analysis of the data with R. Finally, thanks to Mylène M Mariette, who kindly accepted to read and correct this manuscript.

This study is funded by the French Agence Nationale de la Recherche (A.N.R., project “BIRDS’VOICE”) and Saint-Etienne Métropole. C.V. is supported by a Young Investigator Sabbatical of the Université de Saint-Etienne. N.M. is supported by the Institut universitaire de France and was funded during part of this study by the Miller Institute for Basic Research in Science, University of California, Berkeley (Visiting Miller Professorship). J.E.E. is supported by the French Ministry of Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julie E. Elie.

Additional information

Communicated by I. Hartley

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elie, J.E., Mathevon, N. & Vignal, C. Same-sex pair-bonds are equivalent to male–female bonds in a life-long socially monogamous songbird. Behav Ecol Sociobiol 65, 2197–2208 (2011). https://doi.org/10.1007/s00265-011-1228-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-011-1228-9

Keywords

Navigation