Genetica

, Volume 134, Issue 1, pp 147–158 | Cite as

Female choice for genetic complementarity in birds: a review

  • Herman L. MaysJr.
  • Tomas Albrecht
  • Mark Liu
  • Geoffrey E. Hill
Article

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.

Keywords

Aves Female mate choice Genetic compatibility Genetic complementarity Heterosis Heterozygosity Sexual selection 

References

  1. 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 54:119–126Google Scholar
  2. Albrecht T, Schnitzer J, Kreisinger J et al (2007) Extrapair paternity and the opportunity for sexual selection in long-distant migratory passerines. Behav Ecol 18:477–486Google Scholar
  3. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  4. Andersson M, Ahlund M (2000) Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird. Proc Natl Acad Sci USA 97:13188–13193PubMedGoogle Scholar
  5. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302PubMedGoogle Scholar
  6. 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 13:591–597Google Scholar
  7. Barber CA, Edwards MJ, Robertson RJ (2005) A test of the genetic compatibility hypothesis with tree swallows Tachycineta bicolor. Can J Zool 83:955–961Google Scholar
  8. Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford University Press, OxfordGoogle Scholar
  9. Blomqvist D, Andersson M, Kupper C et al (2002) Genetic similarity between mates and extra-pair parentage in three species of shorebirds. Nature 419:613–615PubMedGoogle Scholar
  10. 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 142:1133–1148Google Scholar
  11. Bonduriansky R (2001) The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev 76:305–339PubMedGoogle Scholar
  12. Bonneaud C, Chastel O, Federici P et al (2006) Complex Mhc-based mate choice in a wild passerine. Proc Roy Soc Lond B 273:1111–1116Google Scholar
  13. 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 15:2589–2600PubMedGoogle Scholar
  14. 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 271:159–164Google Scholar
  15. Brown JL (1997) A theory of mate choice based on heterozygosity. Behav Ecol 8:60–65Google Scholar
  16. Charlesworth B, Charlesworth D (1999) The genetic basis of inbreeding depression. Genet Res 74:329–340PubMedGoogle Scholar
  17. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268Google Scholar
  18. 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 35:524–532Google Scholar
  19. Cohen LB, Dearborn DC (2004) Great frigatebirds, Fregata minor, choose mates that are genetically similar. Anim Behav 68:1229–1236Google Scholar
  20. Colegrave N, Kotiaho JS, Tomkins JL (2002) Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evol Ecol Res 4:911–917Google Scholar
  21. Darwin C (1871) The Descent of Man and Selection in Relation to Sex. Princeton University Press, PrincetonGoogle Scholar
  22. Edly-Wright C, Schwagmeyer PL, Parker PG et al (2007) Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows. Anim Behav 73:367–378Google Scholar
  23. Eimes JA, Parker PG, Brown JL et al (2005) Extrapair fertilization and genetic similarity of social mates in the Mexican jay. Behav Ecol 16:456–460Google Scholar
  24. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  25. Foerster K, Delhey K, Johnsen A et al (2003) Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714–717PubMedGoogle Scholar
  26. 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 15:4555–4567PubMedGoogle Scholar
  27. Forstmeier W, Birkhead TR (2004) Repeatability of mate choice in the zebra finch: consistency within and between females. Anim Behav 68:1017–1028Google Scholar
  28. 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 12:3077–3083PubMedGoogle Scholar
  29. Freeman-Gallant CR, Wheelwright NT, Meiklejohn KE et al (2006) Genetic similarity, extrapair paternity, and offspring quality in Savannah sparrows (Passerculus sandwichensis). Behav Ecol 17:952–958Google Scholar
  30. Garner TWJ, Schmidt BR (2003) Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proc Roy Soc Lond B 270:619–624Google Scholar
  31. Garvin JC, Abroe B, Pedersen MC et al (2006) Immune response of nestling warblers varies with extra-pair paternity and temperature. Mol Ecol 15:3833–3840PubMedGoogle Scholar
  32. Grant PR, Grant BR, Keller LF et al (2003) Inbreeding and interbreeding in Darwin’s finches. Evolution 57:2911–2916PubMedGoogle Scholar
  33. Hansson B, Bensch S, Hasselquist D et al (2001) Microsatellite diversity predicts recruitment of sibling great reed warblers. Proc Roy Soc Lond B 268:1287–1291Google Scholar
  34. 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–S292Google Scholar
  35. Hasselquist D, Bensch S, von Schantz T (1995) Low frequency of extra-pair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus. Behav Ecol 6:27–38Google Scholar
  36. Hatchwell BJ, Ross DJ, Fowlie MK et al (2001) Kin discrimination in cooperatively breeding long-tailed tits. Proc Roy Soc Lond B 268:885–890Google Scholar
  37. Hawley DM, Sydenstricker KV, Kollias GV et al (2005) Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches. Biol Lett 1:326–329PubMedGoogle Scholar
  38. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339Google Scholar
  39. Hunt J, Bussiere LF, Jennions MD et al (2004) What is genetic quality? Trends Ecol Evol 19:329–333PubMedGoogle Scholar
  40. Jamieson IG, Roy MS, Lettink M (2003) Sex-specific consequences of recent inbreeding in an ancestrally inbred population of New Zealand Takahe. Conserv Biol 17:708–716Google Scholar
  41. Johnsen A, Andersen V, Sunding C et al (2000) Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature 406:296–299PubMedGoogle Scholar
  42. Kleven O, Lifjeld JT (2004) Extrapair paternity and offspring immunocompetence in the reed bunting, Emberiza schoeniclus. Anim Behav 68:283–289Google Scholar
  43. Kleven O, Lifjeld JT (2005) No evidence for increased offspring heterozygosity from extrapair mating in the reed bunting (Emberiza schoeniclus). Behav Ecol 16:561–565Google Scholar
  44. Kleven O, Jacobsen F, Robertson RJ et al (2005) Extrapair mating between relatives in the barn swallow: a role for kin selection? Biol Lett 1:389–392PubMedGoogle Scholar
  45. 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 71:839–845Google Scholar
  46. 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 59:412–418Google Scholar
  47. Kokko H, Brooks R, McNamara JM et al (2002) The sexual selection continuum. Proc Roy Soc Lond B 269:1331–1340Google Scholar
  48. 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 271:963–969Google Scholar
  49. 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 137:1317–1330Google Scholar
  50. 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 57:32–39Google Scholar
  51. Lehmann L, Keller LF, Kokko H (2007) Mate choice evolution, dominance effects, and the maintenance of genetic variation. J Theor Biol 244:282–295PubMedGoogle Scholar
  52. MacDougall-Shackleton EA, Derryberry EP, Foufopoulos J et al (2005) Parasite-mediated heterozygote advantage in an outbred songbird population. Biol Lett 1:105–107PubMedGoogle Scholar
  53. 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 92:306–315PubMedGoogle Scholar
  54. 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 56:131–142PubMedGoogle Scholar
  55. Marshall RC, Buchanan KL, Catchpole CK (2003) Sexual selection and individual genetic diversity in a songbird. Proc Roy Soc Lond B (Suppl.) 270:S248–250Google Scholar
  56. 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 270:1393–1397Google Scholar
  57. Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559PubMedGoogle Scholar
  58. Mead LS, Arnold SJ (2004) Quantitative genetic models of sexual selection. Trends Ecol Evol 19:264–271PubMedGoogle Scholar
  59. Milinski M (2003) The function of mate choice in sticklebacks: optimizing Mhc genetics. J Fish Biol 63:1–16Google Scholar
  60. Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol Syst 37:159–186Google Scholar
  61. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 14:19–38PubMedGoogle Scholar
  62. Oh KP, Badyaev AV (2006) Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. Proc Roy Soc Lond B 273:1913–1919Google Scholar
  63. 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–S256Google Scholar
  64. 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 32:338–344Google Scholar
  65. Pemberton J (2004) Measuring inbreeding depression in the wild: the old ways are the best. Trends Ecol Evol 19:613–615PubMedGoogle Scholar
  66. Penn DJ (2002) The scent of genetic compatibility: Sexual selection and the major histocompatibility complex. Ethology 108:1–21Google Scholar
  67. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153:145–164Google Scholar
  68. Petrie M, Kempenaers B (1998) Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol Evol 13:52–58Google Scholar
  69. Pialek J, Albrecht T (2005) Choosing mates: complementary versus compatible genes. Trends Ecol Evol 20:63PubMedGoogle Scholar
  70. Pizzari T, Lovlie H, Cornwallis CK (2004) Sex-specific, counteracting responses to inbreeding in a bird. Proc Roy Soc Lond B 271:2115–2121Google Scholar
  71. Puurtinen M, Ketola T, Kotiaho JS (2005) Genetic compatibility and sexual selection. Trends Ecol Evol 20:157–158PubMedGoogle Scholar
  72. Rätti O, Hovi M, Lundberg A et al (1995) Extra-pair paternity and male characteristics in the Pied Flycatcher. Behav Ecol Sociobiol 37:419–425Google Scholar
  73. 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 270:2151–2157Google Scholar
  74. 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 272:481–487Google Scholar
  75. Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the Seychelles warbler: Environment-dependent maternal effects. Evolution 58:2037–2048PubMedGoogle Scholar
  76. 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 272:759–767Google Scholar
  77. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genet 35:103–106PubMedGoogle Scholar
  78. 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 69:1013–1022Google Scholar
  79. 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 271:1823–1829Google Scholar
  80. Shuster SM, Wade MJ (2003) Mating Systems and Strategies. Princeton University Press, Princeton, New JerseyGoogle Scholar
  81. Slate J, Pemberton JM (2002) Comparing molecular measures for detecting inbreeding depression. J Evol Biol 15:20–31Google Scholar
  82. 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 93:255–265PubMedGoogle Scholar
  83. 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 36:146–154Google Scholar
  84. Spottiswoode C, Møller AP (2004) Genetic similarity and hatching success in birds. Proc Roy Soc Lond B 271:267–272Google Scholar
  85. Stapleton MK, Kleven O, Lifjeld JT, Robertson RJ (2007) Female tree swallows (Tachycineta bicolor) increase offspring heterozygosity through extrapair mating. Behav Ecol Sociobiol 61:1725–1733Google Scholar
  86. 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 108:399–413Google Scholar
  87. 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 7:353–364Google Scholar
  88. Tang-Martinez Z, Ryder TB (2005) The problem with paradigms: Bateman’s worldview as a case study. Integr Comp Biol 45:821–830Google Scholar
  89. 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 70:945–955Google Scholar
  90. Thuman KA, Griffith SC (2005) Genetic similarity and the nonrandom distribution of paternity in a genetically highly polyandrous shorebird. Anim Behav 69:765–770Google Scholar
  91. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027PubMedGoogle Scholar
  92. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Aldine Publishing Company, ChicagoGoogle Scholar
  93. Van Rhijn JG (1991) The Ruff. T&AD Poyser Ltd., LondonGoogle Scholar
  94. Weatherhead PJ, Dufour KW, Lougheed SC et al (1999) A test of the good-genes-as-heterozygosity hypothesis using red-winged blackbirds. Behav Ecol 10:619–625Google Scholar
  95. Wedekind C, Seebeck T, Bettens F et al (1995) Mhc-dependent mate preferences in humans. Proc Roy Soc Lond B 260:245–249Google Scholar
  96. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: Causes, correlates, and conflict. Ann Rev Ecol Evol Syst 34:365–396Google Scholar
  97. Whittingham LA, Dunn PO (2005) Effects of extra-pair and within-pair reproductive success on the opportunity for selection in birds. Behav Ecol 16:138–144Google Scholar
  98. Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15:841–849PubMedGoogle Scholar
  99. Zahavi A (1975) Mate selection – selection for a handicap. J Theor Biol 53:205–214PubMedGoogle Scholar
  100. Zeh JA, Zeh DW (1996) The evolution of polyandry I: Intragenomic conflict and genetic incompatibility. Proc Roy Soc Lond B 263:1711–1717Google Scholar
  101. Zeh JA, Zeh DW (2003) Toward a new sexual selection paradigm: Polyandry, conflict and incompatibility (Invited article). Ethology 109:929–950Google Scholar
  102. 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–S237Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Herman L. MaysJr.
    • 1
    • 2
  • Tomas Albrecht
    • 3
    • 4
  • Mark Liu
    • 1
  • Geoffrey E. Hill
    • 1
  1. 1.Department of BiologyAuburn UniversityAuburnUSA
  2. 2.Cincinnati Museum CenterCincinnatiUSA
  3. 3.Institute of Vertebrate Biology v.v.iAcademy of Sciences of the Czech RepublicStudenec 122Czech Republic
  4. 4.Department of ZoologyCharles University in PraguePragueCzech Republic

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