Skip to main content
SpringerLink
Log in

Female choice for genetic complementarity in birds: a review

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Data from avian species have played a prominent role in developing and testing theories of female mate choice. One of the most prominent models of sexual selection, the “good genes” model, emphasizes the indirect benefits of female preferences for male ornaments as indicators of a potential sire’s additive genetic quality. However, there is growing interest in non-additive sources of genetic quality and mate choice models for self-referential disassortative mating based on optimal levels of genetic dissimilarity. We reviewed the empirical evidence for genetic-complementarity-based female mate choice among birds. We found the evidence for such choice is mixed but in general against the genetic complementarity hypothesis. The lack of evidence for genetic complementarity in many birds may be due to an inability to make the fine distinctions among potential mates based on genes, possibly due to the comparative anosmatic nature of avian sensory system. For some species however there is compelling evidence for genetic complementarity as a criterion used in female mate choice. Understanding the ubiquity of female mate choice based on genetic complementarity and the variation in this source of female preference among and within species remains a challenge.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aeschlimann PB, Haberli MA, Reusch TBH et al (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimize MHC allele number during mate selection. Behav Ecol Sociobiol 54:119–126

    Google Scholar 

  • Albrecht T, Schnitzer J, Kreisinger J et al (2007) Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav Ecol 18:477–486

    Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  • Andersson M, Ahlund M (2000) Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird. Proc Natl Acad Sci USA 97:13188–13193

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Badyaev AV, Hill GE (2002) Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch. Behav Ecol 13:591–597

    Google Scholar 

  • Barber CA, Edwards MJ, Robertson RJ (2005) A test of the genetic compatibility hypothesis with tree swallows Tachycineta bicolor. Can J Zool 83:955–961

    CAS  Google Scholar 

  • Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford University Press, Oxford

    Google Scholar 

  • Blomqvist D, Andersson M, Kupper C et al (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615

    PubMed  CAS  Google Scholar 

  • Blomqvist D, Fessl B, Hoi H et al (2005) High frequency of extra-pair fertilisations in the moustached warbler, a songbird with a variable breeding system. Behaviour 142:1133–1148

    Google Scholar 

  • Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339

    PubMed  CAS  Google Scholar 

  • Bonneaud C, Chastel O, Federici P et al (2006) Complex Mhc-based mate choice in a wild passerine. Proc Roy Soc Lond B 273:1111–1116

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Bretman A, Wedell N, Tregenza T (2004) Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc Roy Soc Lond B 271:159–164

    CAS  Google Scholar 

  • Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65

    Google Scholar 

  • Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340

    PubMed  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Google Scholar 

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

    Google Scholar 

  • Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68:1229–1236

    Google Scholar 

  • Colegrave N, Kotiaho JS, Tomkins JL (2002) Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evol Ecol Res 4:911–917

    Google Scholar 

  • Darwin C (1871) The Descent of Man and Selection in Relation to Sex. Princeton University Press, Princeton

    Google Scholar 

  • Edly-Wright C, Schwagmeyer PL, Parker PG et al (2007) Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows. Anim Behav 73:367–378

    Google Scholar 

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

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Foerster K, Valcu M, Johnsen A et al (2006) A spatial genetic structure and effects of relatedness on mate choice in a wild bird population. Mol Ecol 15:4555–4567

    PubMed  CAS  Google Scholar 

  • Forstmeier W, Birkhead TR (2004) Repeatability of mate choice in the zebra finch: consistency within and between females. Anim Behav 68:1017–1028

    Google Scholar 

  • Freeman-Gallant CR, Meguerdichian M, Wheelwright NT et al (2003) Social pairing and female mating fidelity predicted by restriction fragment length polymorphism similarity at the major histocompatibility complex in a songbird. Mol Ecol 12:3077–3083

    PubMed  Google Scholar 

  • Freeman-Gallant CR, Wheelwright NT, Meiklejohn KE et al (2006) Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis). Behav Ecol 17:952–958

    Google Scholar 

  • Garner TWJ, Schmidt BR (2003) Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proc Roy Soc Lond B 270:619–624

    Google Scholar 

  • Garvin JC, Abroe B, Pedersen MC et al (2006) Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol Ecol 15:3833–3840

    PubMed  CAS  Google Scholar 

  • Grant PR, Grant BR, Keller LF et al (2003) Inbreeding and interbreeding in Darwin’s finches. Evolution 57:2911–2916

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hansson B, Hasselquist D, Bensch S (2004) Do female great reed warblers seek extra-pair fertilizations to avoid inbreeding? Proc Roy Soc Lond B (Suppl.) 271:S290–S292

    Google Scholar 

  • Hasselquist D, Bensch S, von Schantz T (1995) Low frequency of extra-pair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus. Behav Ecol 6:27–38

    Google Scholar 

  • Hatchwell BJ, Ross DJ, Fowlie MK et al (2001) Kin discrimination in cooperatively breeding long-tailed tits. Proc Roy Soc Lond B 268:885–890

    CAS  Google Scholar 

  • Hawley DM, Sydenstricker KV, Kollias GV et al (2005) Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biol Lett 1:326–329

    PubMed  Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339

    Google Scholar 

  • Hunt J, Bussiere LF, Jennions MD et al (2004) What is genetic quality? Trends Ecol Evol 19:329–333

    PubMed  Google Scholar 

  • Jamieson IG, Roy MS, Lettink M (2003) Sex-specific consequences of recent inbreeding in an ancestrally inbred population of New Zealand Takahe. Conserv Biol 17:708–716

    Google Scholar 

  • Johnsen A, Andersen V, Sunding C et al (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299

    PubMed  CAS  Google Scholar 

  • Kleven O, Lifjeld JT (2004) Extrapair paternity and offspring immunocompetence in the reed bunting, Emberiza schoeniclus. Anim Behav 68:283–289

    Google Scholar 

  • Kleven O, Lifjeld JT (2005) No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus). Behav Ecol 16:561–565

    Google Scholar 

  • Kleven O, Jacobsen F, Robertson RJ et al (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392

    PubMed  Google Scholar 

  • Kleven O, Jacobsen F, Izadnegahdar R et al (2006a) No evidence of paternal genetic contribution to nestling cell-mediated immunity in the North American barn swallow. Anim Behav 71:839–845

    Google Scholar 

  • Kleven O, Jacobsen F, Izadnegahdar R et al (2006b) Male streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster). Behav Ecol Sociobiol 59:412–418

    Google Scholar 

  • Kokko H, Brooks R, McNamara JM et al (2002) The sexual selection continuum. Proc Roy Soc Lond B 269:1331–1340

    Google Scholar 

  • Komdeur J, Richardson DS, Burke T (2004) Experimental evidence that kin discrimination in the Seychelles warbler is based on association and not on genetic relatedness. Proc Roy Soc Lond B 271:963–969

    Google Scholar 

  • 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 137:1317–1330

    Google Scholar 

  • Kupper C, Kis J, Kosztolanyi A et al (2004) Genetic mating system and timing of extra-pair fertilizations in the Kentish plover. Behav Ecol Sociobiol 57:32–39

    Google Scholar 

  • Lehmann L, Keller LF, Kokko H (2007) Mate choice evolution, dominance effects, and the maintenance of genetic variation. J Theor Biol 244:282–295

    PubMed  CAS  Google Scholar 

  • MacDougall-Shackleton EA, Derryberry EP, Foufopoulos J et al (2005) Parasite-mediated heterozygote advantage in an outbred songbird population. Biol Lett 1:105–107

    PubMed  Google Scholar 

  • Markert JA, Grant PR, Grant B et al (2004) Neutral locus heterozygosity, inbreeding, and survival in Darwin’s ground finches (Geospiza fortis and G. scandens). Heredity 92:306–315

    PubMed  CAS  Google Scholar 

  • Marr AB, Keller LF, Arcese P (2002) Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia). Evolution 56:131–142

    PubMed  Google Scholar 

  • Marshall RC, Buchanan KL, Catchpole CK (2003) Sexual selection and individual genetic diversity in a songbird. Proc Roy Soc Lond B (Suppl.) 270:S248–250

    Google Scholar 

  • Masters BS, Hicks BG, Johnson LS et al (2003) Genotype and extra-pair paternity in the house wren: a rare-male effect? Proc Roy Soc Lond B 270:1393–1397

    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 

  • Mead LS, Arnold SJ (2004) Quantitative genetic models of sexual selection. Trends Ecol Evol 19:264–271

    PubMed  Google Scholar 

  • Milinski M (2003) The function of mate choice in sticklebacks: optimizing Mhc genetics. J Fish Biol 63:1–16

    Google Scholar 

  • Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186

    Google Scholar 

  • Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38

    PubMed  CAS  Google Scholar 

  • Oh KP, Badyaev AV (2006) Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. Proc Roy Soc Lond B 273:1913–1919

    Google Scholar 

  • Olsson M, Madsen T, Nordby J et al (2003) Major histocompatibility complex and mate choice in sand lizards. Proc Roy Soc Lond B (Suppl.) 270:S254–S256

    CAS  Google Scholar 

  • Otter KA, Stewart IRK, McGregor PK et al (2001) Extra-pair paternity among Great Tits, Parus major, following manipulation of male signals. J Avian Biol 32:338–344

    Google Scholar 

  • Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615

    PubMed  Google Scholar 

  • Penn DJ (2002) The scent of genetic compatibility: Sexual selection and the major histocompatibility complex. Ethology 108:1–21

    Google Scholar 

  • Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164

    Google Scholar 

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

    Google Scholar 

  • Pialek J, Albrecht T (2005) Choosing mates: complementary versus compatible genes. Trends Ecol Evol 20:63

    PubMed  Google Scholar 

  • Pizzari T, Lovlie H, Cornwallis CK (2004) Sex-specific, counteracting responses to inbreeding in a bird. Proc Roy Soc Lond B 271:2115–2121

    Google Scholar 

  • Puurtinen M, Ketola T, Kotiaho JS (2005) Genetic compatibility and sexual selection. Trends Ecol Evol 20:157–158

    PubMed  Google Scholar 

  • Rätti O, Hovi M, Lundberg A et al (1995) Extra-pair paternity and male characteristics in the Pied Flycatcher. Behav Ecol Sociobiol 37:419–425

    Google Scholar 

  • Reid JM, Arcese P, Keller LF (2003) Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects. Proc Roy Soc Lond B 270:2151–2157

    Google Scholar 

  • Reid JM, Arcese P, Cassidy ALEV et al (2005) Hamilton and Zuk meet heterozygosity? Song repertoire size indicates inbreeding and immunity in song sparrows (Melospiza melodia). Proc Roy Soc Lond B 272:481–487

    Google Scholar 

  • Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the Seychelles warbler: Environment-dependent maternal effects. Evolution 58:2037–2048

    PubMed  Google Scholar 

  • Richardson DS, Komdeur J, Burke T et al (2005) MHC-based patterns of social and extra-pair mate choice in the Seychelles warbler. Proc Roy Soc Lond B 272:759–767

    Google Scholar 

  • Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genet 35:103–106

    PubMed  CAS  Google Scholar 

  • Schmoll T, Quellmalz A, Dietrich V et al (2005) Genetic similarity between pair mates is not related to extrapair paternity in the socially monogamous coal tit. Anim Behav 69:1013–1022

    Google Scholar 

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

    Google Scholar 

  • Shuster SM, Wade MJ (2003) Mating Systems and Strategies. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. J Evol Biol 15:20–31

    Google Scholar 

  • Slate J, David P, Dodds KG et al (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265

    PubMed  CAS  Google Scholar 

  • Smith SB, Webster MS, Holmes RT (2005) The heterozygosity theory of extra-pair mate choice in birds: a test and a cautionary note. J Avian Biol 36:146–154

    Google Scholar 

  • Spottiswoode C, Møller AP (2004) Genetic similarity and hatching success in birds. Proc Roy Soc Lond B 271:267–272

    Google Scholar 

  • Stapleton MK, Kleven O, Lifjeld JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733

    Google Scholar 

  • Stewart IRK, Hanschu RD, Burke T et al (2006) Tests of ecological, phenotypic, and genetic correlates of extra-pair paternity in the House Sparrow. Condor 108:399–413

    Google Scholar 

  • Swinnerton KJ, Groombridge JJ, Jones CG et al (2004) Inbreeding depression and founder diversity among captive and free-living populations of the endangered pink pigeon Columba mayeri. Anim Conserv 7:353–364

    Google Scholar 

  • Tang-Martinez Z, Ryder TB (2005) The problem with paradigms: Bateman’s worldview as a case study. Integr Comp Biol 45:821–830

    Google Scholar 

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

    Google Scholar 

  • Thuman KA, Griffith SC (2005) Genetic similarity and the nonrandom distribution of paternity in a genetically highly polyandrous shorebird. Anim Behav 69:765–770

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Aldine Publishing Company, Chicago

    Google Scholar 

  • Van Rhijn JG (1991) The Ruff. T&AD Poyser Ltd., London

    Google Scholar 

  • Weatherhead PJ, Dufour KW, Lougheed SC et al (1999) A test of the good-genes-as-heterozygosity hypothesis using red-winged blackbirds. Behav Ecol 10:619–625

    Google Scholar 

  • Wedekind C, Seebeck T, Bettens F et al (1995) Mhc-dependent mate preferences in humans. Proc Roy Soc Lond B 260:245–249

    CAS  Google Scholar 

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

    Google Scholar 

  • Whittingham LA, Dunn PO (2005) Effects of extra-pair and within-pair reproductive success on the opportunity for selection in birds. Behav Ecol 16:138–144

    Google Scholar 

  • Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15:841–849

    PubMed  Google Scholar 

  • Zahavi A (1975) Mate selection – selection for a handicap. J Theor Biol 53:205–214

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: Polyandry, conflict and incompatibility (Invited article). Ethology 109:929–950

    Google Scholar 

  • Zelano B, Edwards SV (2002) An Mhc component to kin recognition and mate choice in birds: Predictions, progress, and prospects. Am Nat (Suppl.) 160:S225–S237

    Google Scholar 

Download references

Acknowledgements

Thanks to two anonymous referees who contributed very useful comments to this manuscript. HLM, ML and GEH were supported under National Science Foundation Grant #NSF-IBN0235778 and TA was supported through funding from Charles University in Prague and The Academy of Sciences of the Czech Republic, and the Grant Agency of the Czech Republic (MSMT 0021620828, AV0Z60930519 and 206/06/0851).

Author information

Author notes

  1. Herman L. Mays Jr.

    Present address: Cincinnati Museum Center, 1301 Western Avenue, Cincinnati, OH, 45203, USA

Authors and Affiliations

  1. Department of Biology, Auburn University, Auburn, AL, 36830, USA

    Herman L. Mays Jr., Mark Liu & Geoffrey E. Hill

  2. Institute of Vertebrate Biology v.v.i, Academy of Sciences of the Czech Republic, Studenec 122, CZ 67502, Czech Republic

    Tomas Albrecht

  3. Department of Zoology, Charles University in Prague, Prague, CZ 12844, Czech Republic

    Tomas Albrecht

Authors
  1. Herman L. Mays Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomas Albrecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Geoffrey E. Hill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Herman L. Mays Jr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mays, H.L., Albrecht, T., Liu, M. et al. Female choice for genetic complementarity in birds: a review. Genetica 134, 147–158 (2008). https://doi.org/10.1007/s10709-007-9219-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9219-5

Keywords

Search

Navigation