The Bees Do It, but What About the Birds? Evidence for Sex Ratio Adjustment in Birds

  • Kristen J. Navara
Part of the Fascinating Life Sciences book series (FLS)


In birds, the female is responsible for determining the sexes of her offspring, and she accomplishes this by donating either a W or a Z chromosome to the egg. There is now a large body of evidence that female birds can adjust which sex chromosome the eggs receive in response to the social and/or environmental conditions surrounding them. In this chapter, I highlight the many factors that have been shown to influence avian sex ratios and highlight the need for a multipronged approach incorporating multiple life history traits when attempting to understand the adaptive significance of sex allocation in birds.


  1. Abroe B, Garvin JC, Pedersen MC, Whittingham LA, Dunn PO, Lank D (2007) Brood sex ratios are related to male size but not to attractiveness in common yellowthroats (Geothlypis trichas). Auk 124(1):176–184CrossRefGoogle Scholar
  2. Alonso-Alvarez C, Doutrelant C, Sorci G (2004) Ultraviolet reflectance affects male-male interactions in the blue tit (Parus caeruleus ultramarinus). Behav Ecol 15(5):805–809CrossRefGoogle Scholar
  3. Anderson D, Reeve J, Bird D (1997) Sexually dimorphic eggs, nestling growth and sibling competition in American kestrels Falco sparverius. Funct Ecol 11(3):331–335CrossRefGoogle Scholar
  4. Arnold KE, Griffiths R, Stevens DJ, Orr KJ, Adam A, Houston DC (2003) Subtle manipulation of egg sex ratio in birds. Proc R Soc Lond B Biol Sci 270(Suppl 2):S216–S219CrossRefGoogle Scholar
  5. Badyaev AV, Hill GE, Beck ML, Dervan AA, Duckworth RA, McGraw KJ, Nolan PM, Whittingham LA (2002) Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295(5553):316–318CrossRefPubMedGoogle Scholar
  6. Blanchard P, Hanuise N, Dano S, Weimerskirch H (2007) Offspring sex ratio in relation to parental structural size and body condition in the long-lived wandering albatross (Diomedea exulans). Behav Ecol Sociobiol 61(5):767–773CrossRefGoogle Scholar
  7. Booksmyth I, Mautz B, Davis J, Nakagawa S, Jennions MD (2015) Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta-analysis. Biol Rev 92:108–134CrossRefGoogle Scholar
  8. Bortolotti GR (1986a) Evolution of growth rates in eagles: sibling competition vs. energy considerations. Ecology 67(1):182–194CrossRefGoogle Scholar
  9. Bortolotti GR (1986b) Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am Nat:495–507Google Scholar
  10. Bradbury R, Blakey J (1998) Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata. Proc R Soc Lond B Biol Sci 265(1399):895–899CrossRefGoogle Scholar
  11. Brommer JE, Karell P, Pihlaja T, Painter JN, Primmer CR, Pietiäinen H (2003) Ural owl sex allocation and parental investment under poor food conditions. Oecologia 137(1):140–147CrossRefPubMedGoogle Scholar
  12. Burley N (1981) Sex ratio manipulation and selection for attractiveness. Science 211(4483):721–722CrossRefPubMedGoogle Scholar
  13. Burley N (1986) Sex-ratio manipulation in color-banded populations of zebra finches. Evolution:1191–1206Google Scholar
  14. Cassey P, Ewen JG, Møller AP (2006) Revised evidence for facultative sex ratio adjustment in birds: a correction. Proc R Soc Lond B Biol Sci 273(1605):3129–3130CrossRefGoogle Scholar
  15. Clout MN, Elliott GP, Robertson BC (2002) Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous parrot. Biol Conserv 107(1):13–18CrossRefGoogle Scholar
  16. Cordero P, Vinuela J, Aparicio J, Veiga J (2001) Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J Evol Biol 14(5):829–834CrossRefGoogle Scholar
  17. Daan S, Dijkstra C, Weissing FJ (1996) An evolutionary explanation for seasonal trends in avian sex ratios. Behav Ecol 7(4):426–430CrossRefGoogle Scholar
  18. Dawson RD, Bortolotti GR (1997) Total plasma protein level as an indicator of condition in wild American kestrels (Falco sparverius). Can J Zool 75(5):680–686CrossRefGoogle Scholar
  19. Delhey K, Peters A, Johnsen A, Kempenaers B (2007) Brood sex ratio and male UV ornamentation in blue tits (Cyanistes caeruleus): correlational evidence and an experimental test. Behav Ecol Sociobiol 61(6):853–862CrossRefGoogle Scholar
  20. Delmore KE, Kleven O, Laskemoen T, Crowe SA, Lifjeld JT, Robertson RJ (2008) Sex allocation and parental quality in tree swallows. Behav Ecol 19(6):1243–1249CrossRefGoogle Scholar
  21. Dietrich-Bischoff V, Schmoll T, Winkel W, Krackow S, Lubjuhn T (2006) Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater). Behav Ecol Sociobiol 60(4):563–571CrossRefGoogle Scholar
  22. Dijkstra C, Daan S, Buker J (1990) Adaptive seasonal variation in the sex ratio of kestrel broods. Funct Ecol 4:143–147CrossRefGoogle Scholar
  23. Donald PF (2007) Adult sex ratios in wild bird populations. Ibis 149(4):671–692CrossRefGoogle Scholar
  24. Dreiss A, Richard M, Moyen F, White J, Møller A, Danchin E (2006) Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus. Behav Ecol 17(1):13–19CrossRefGoogle Scholar
  25. Dubois NS, Kennedy ED, Getty T (2006) Surplus nest boxes and the potential for polygyny affect clutch size and offspring sex ratio in house wrens. Proc R Soc Lond B Biol Sci 273(1595):1751–1757CrossRefGoogle Scholar
  26. Dzus EH, Bortolotti GR, Gerrard JM (1996) Does sex-biased hatching order in bald eagles vary with food resources? Ecoscience 3(3):252–258CrossRefGoogle Scholar
  27. Ellegren H, Gustafsson L, Sheldon BC (1996) Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci 93(21):11723–11728CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ewen JG (2003) Facultative control of offspring sex in the cooperatively breeding bell miner, Manorina melanophrys. Behav Ecol 14(2):157–164CrossRefGoogle Scholar
  29. Gebhardt-Henrich SG, Van Noordwijk AJ (1991) Nestling growth in the great tit I. Heritability estimates under different environmental conditions. J Evol Biol 4(3):341–362CrossRefGoogle Scholar
  30. Genovart M, Oro D, Ruiz X, Griffiths R, Monaghan P, Nager RG (2003) Seasonal changes in brood sex composition in Audouin’s Gulls. Condor 105(4):783–790CrossRefGoogle Scholar
  31. Graham EB, Caro SP, Sockman KW (2011) Change in offspring sex ratio over a very short season in Lincoln’s Sparrows: the potential role of bill development. J Field Ornithol 82(1):44–51CrossRefGoogle Scholar
  32. Griffin AS, Sheldon BC, West SA (2005) Cooperative breeders adjust offspring sex ratios to produce helpful helpers. Am Nat 166(5):628–632CrossRefPubMedGoogle Scholar
  33. Griffith S, Örnborg J, Russell A, Andersson S, Sheldon B (2003) Correlations between ultraviolet coloration, overwinter survival and offspring sex ratio in the blue tit. J Evol Biol 16(5):1045–1054CrossRefPubMedGoogle Scholar
  34. Griggio M, Hamerstrom F, Rosenfield RN, Tavecchia G (2002) Seasonal variation in sex ratio of fledgling American Kestrels: a long term study. Wilson Bull 114(4):474–478CrossRefGoogle Scholar
  35. Heinsohn R, Legge S, Barry S (1997) Extreme bias in sex allocation in Eclectusparrots. Proc R Soc Lond B Biol Sci 264(1386):1325–1329CrossRefGoogle Scholar
  36. Hipkiss T, Hörnfeldt B (2004) High interannual variation in the hatching sex ratio of Tengmalm’s owl broods during a vole cycle. Popul Ecol 46(3):263–268CrossRefGoogle Scholar
  37. Hunt S, Bennett AT, Cuthill IC, Griffiths R (1998) Blue tits are ultraviolet tits. Proc R Soc Lond B Biol Sci 265(1395):451–455CrossRefGoogle Scholar
  38. Hunt S, Cuthill IC, Bennett AT, Griffiths R (1999) Preferences for ultraviolet partners in the blue tit. Anim Behav 58(4):809–815CrossRefPubMedGoogle Scholar
  39. Husby A, Sæther BE, Jensen H, Ringsby TH (2006) Causes and consequences of adaptive seasonal sex ratio variation in house sparrows. J Anim Ecol 75(5):1128–1139CrossRefPubMedGoogle Scholar
  40. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B Biol Sci 270(1521):1263–1270CrossRefGoogle Scholar
  41. Kalmbach E, Nager RG, Griffiths R, Furness RW (2001) Increased reproductive effort results in male-biased offspring sex ratio: an experimental study in a species with reversed sexual size dimorphism. Proc R Soc Lond B Biol Sci 268(1481):2175–2179CrossRefGoogle Scholar
  42. Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56(1):155–164CrossRefPubMedGoogle Scholar
  43. Koenig WD, Dickinson JL (1996) Nestling sex-ratio variation in Western Bluebirds. Auk:902–910Google Scholar
  44. Kölliker M, Heeb P, Werner I, Mateman A, Lessells C, Richner H (1999) Offspring sex ratio is related to male body size in the great tit (Parus major). Behav Ecol 10(1):68–72CrossRefGoogle Scholar
  45. Komdeur J, Pen I (2002) Adaptive sex allocation in birds: the complexities of linking theory and practice. Phil Trans R Soc Lond B Biol Sci 357(1419):373–380CrossRefGoogle Scholar
  46. Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385(6616):522–525CrossRefGoogle Scholar
  47. Korsten P, Lessells CKM, Mateman AC, Van der Velde M, Komdeur J (2006) Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits. Behav Ecol 17(4):539–546CrossRefGoogle Scholar
  48. Korsten P, Dijkstra TH, Komdeur J (2007) Is UV signalling involved in male-male territorial conflict in the blue tit (Cyanistes caeruleus)? A new experimental approach. Behaviour 144(4):447–470CrossRefGoogle Scholar
  49. Krebs JR (1971) Territory and breeding density in the Great Tit, Parus major L. Ecology 52(1):2–22CrossRefGoogle Scholar
  50. Krebs EA, Green DJ, Double MC, Griffiths R (2002) Laying date and laying sequence influence the sex ratio of crimson rosella broods. Behav Ecol Sociobiol 51(5):447–454CrossRefGoogle Scholar
  51. Leitner S, Marshall RC, Leisler B, Catchpole CK (2006) Male song quality, egg size and offspring sex in captive canaries (Serinus canaria). Ethology 112(6):554–563CrossRefGoogle Scholar
  52. Leroux A, Bretagnolle V (1996) Sex ratio variations in broods of Montagu’s Harriers Circus pygargus. J Avian Biol:63–69Google Scholar
  53. Loyau A, Jalme MS, Sorci G (2005) Intra-and intersexual selection for multiple traits in the peacock (Pavo cristatus). Ethology 111(9):810–820CrossRefGoogle Scholar
  54. Magrath MJ, Green DJ, Komdeur J (2002) Sex allocation in the sexually monomorphic fairy martin. J Avian Biol 33(3):260–268CrossRefGoogle Scholar
  55. Merkling T, Leclaire S, Danchin E, Lhuillier E, Wagner RH, White J, Hatch SA, Blanchard P (2012) Food availability and offspring sex in a monogamous seabird: insights from an experimental approach. Behav Ecol 23:751–758CrossRefGoogle Scholar
  56. Møller AP (1990) Male tail length and female mate choice in the monogamous swallow Hirundo rustica. Anim Behav 39(3):458–465CrossRefGoogle Scholar
  57. Nager R, Monaghan P, Griffiths R, Houston D, Dawson R (1999) Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci 96(2):570–573CrossRefPubMedPubMedCentralGoogle Scholar
  58. Neto JM, Hansson B, Hasselquist D (2011) Sex allocation in Savi’s warblers Locustella luscinioides: multiple factors affect seasonal trends in brood sex ratios. Behav Ecol Sociobiol 65(2):297–304CrossRefGoogle Scholar
  59. Norris K (1990) Female choice and the quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 27(4):275–281CrossRefGoogle Scholar
  60. Norris K (1993) Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 362(6420):537–539CrossRefGoogle Scholar
  61. Okekpe CC (2009) Evidence that maternal diet alters steroid levels and primary offspring sex ratio in the zebra finch. Thesis, Auburn University, AL.Google Scholar
  62. Palmer AR (2000) Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annu Rev Ecol Syst 31:441–480CrossRefGoogle Scholar
  63. Pärt T, Qvarnström A (1997) Badge size in collared flycatchers predicts outcome of male competition over territories. Anim Behav 54(4):893–899CrossRefGoogle Scholar
  64. Petrie M, Cotgreave P, Pike TW (2009) Variation in the peacock’s train shows a genetic component. Genetica 135(1):7–11CrossRefPubMedGoogle Scholar
  65. Pike TW (2005) Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection. Behav Ecol Sociobiol 58(4):407–413CrossRefGoogle Scholar
  66. Pike TW, Petrie M (2005a) Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Anim Behav 70(4):745–751CrossRefGoogle Scholar
  67. Pike TW, Petrie M (2005b) Offspring sex ratio is related to paternal train elaboration and yolk corticosterone in peafowl. Biol Lett 1(2):204–207CrossRefPubMedPubMedCentralGoogle Scholar
  68. Pryke SR, Griffith SC (2009) Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch. Science 323(5921):1605–1607CrossRefPubMedGoogle Scholar
  69. Pryke SR, Rollins LA (2012) Mothers adjust offspring sex to match the quality of the rearing environment. Proc Biol Sci 279(1744):4051–4057CrossRefPubMedPubMedCentralGoogle Scholar
  70. Qvarnström A, Brommer JE, Gustafsson L (2006) Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441(7089):84–86CrossRefPubMedGoogle Scholar
  71. Radford A, Blakey J (2000) Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11(3):294–298CrossRefGoogle Scholar
  72. Rathburn MK, Montgomerie R (2004) Breeding biology and social structure of White-winged Fairy-wrens (Malurus leucopterus): comparison between island and mainland subspecies having different plumage phenotypes. Emu 103(4):295–306CrossRefGoogle Scholar
  73. Rosivall B (2008) Contradictory results in sex ratio studies: populations do not necessarily differ. Behav Ecol Sociobiol 62(6):1037–1042CrossRefGoogle Scholar
  74. Rosivall B, Török J, Hasselquist D, Bensch S (2004) Brood sex ratio adjustment in collared flycatchers (Ficedula albicollis): results differ between populations. Behav Ecol Sociobiol 56(4):346–351CrossRefGoogle Scholar
  75. Rubenstein DR (2007) Temporal but not spatial environmental variation drives adaptive offspring sex allocation in a plural cooperative breeder. Am Nat 170(1):155–165CrossRefPubMedGoogle Scholar
  76. Rutkowska J, Cichoń M (2002) Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim Behav 64(5):817–822CrossRefGoogle Scholar
  77. Rutstein A, Slater P, Graves J (2004) Diet quality and resource allocation in the zebra finch. Proc R Soc Lond B Biol Sci 271(Suppl 5):S286–S289CrossRefGoogle Scholar
  78. Ryder JP (1983) Sex ratio and egg sequence in ring-billed gulls. Auk 100(3):726–728Google Scholar
  79. Saino N, Romano M, Caprioli M, Ambrosini R, Rubolini D, Fasola M (2010) Sex allocation in yellow-legged gulls (Larus michahellis) depends on nutritional constraints on production of large last eggs. Proc R Soc Lond B Biol Sci 277(1685):1203–1208CrossRefGoogle Scholar
  80. Sheldon BC, Andersson S, Griffith SC, Örnborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402(6764):874–877CrossRefGoogle Scholar
  81. Smallwood PD (1998) Seasonal shifts in sex ratios of fledgling American kestrels (Falco sparverius paulus): the early bird hypothesis. Evol Ecol 12(7):839–853CrossRefGoogle Scholar
  82. Sockman KW, Schwabl H (2000) Yolk androgens reduce offspring survival. Proc R Soc Lond B Biol Sci 267(1451):1451–1456CrossRefGoogle Scholar
  83. Suorsa P, Helle H, Huhta E, Jäntti A, Nikula A, Hakkarainen H (2003) Forest fragmentation is associated with primary brood sex ratio in the treecreeper (Certhia familiaris). Proc R Soc Lond B Biol Sci 270(1530):2215–2222CrossRefGoogle Scholar
  84. Svensson E, Nilsson J-A (1996) Mate quality affects offspring sex ratio in blue tits. Proc R Soc Lond B Biol Sci 263(1368):357–361CrossRefGoogle Scholar
  85. Székely T, Cuthill IC, Yezerinac S, Griffiths R, Kis J (2004) Brood sex ratio in the Kentish plover. Behav Ecol 15(1):58–62CrossRefGoogle Scholar
  86. Taff CC, Freeman-Gallant CR, Dunn PO, Whittingham LA (2011) Relationship between brood sex ratio and male ornaments depends on male age in a warbler. Anim Behav 81(3):619–625CrossRefGoogle Scholar
  87. Thuman KA, Widemo F, Griffith SC (2003) Condition-dependent sex allocation in a lek-breeding wader, the ruff (Philomachus pugnax). Mol Ecol 12(1):213–218CrossRefPubMedGoogle Scholar
  88. Torres R, Drummond H (1999) Variably male-biased sex ratio in a marine bird with females larger than males. Oecologia 118(1):16–22CrossRefPubMedGoogle Scholar
  89. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179(4068):90–92CrossRefPubMedGoogle Scholar
  90. Velando A (2002) Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby. Behav Ecol 13(4):443–449CrossRefGoogle Scholar
  91. Velando A, Graves J, Ortega-Ruano JE (2002) Sex ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird. Ibis 144(1):9–16CrossRefGoogle Scholar
  92. West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295(5560):1685–1688CrossRefPubMedGoogle Scholar
  93. Westneat DF, Stewart IR, Woeste EH, Gipson J, Abdulkadir L, Poston JP (2002) Patterns of sex ratio variation in house sparrows. Condor 104(3):598–609CrossRefGoogle Scholar
  94. White K, Eason D, Jamieson I, Robertson B (2015) Evidence of inbreeding depression in the critically endangered parrot, the kakapo. Anim Conserv 18(4):341–347CrossRefGoogle Scholar
  95. Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9(8):1123–1129CrossRefPubMedGoogle Scholar
  96. Whittingham LA, Valkenaar SM, Poirier NE, Dunn PO, Blem C (2002) Maternal condition and nestling sex ratio in house wrens. Auk 119(1):125–131Google Scholar
  97. Wiebe KL, Bortolotti GR (1992) Facultative sex ratio manipulation in American kestrels. Behav Ecol Sociobiol 30(6):379–386CrossRefGoogle Scholar
  98. Wiehn J (1997) Plumage characteristics as an indicator of male parental quality in the American kestrel. J Avian Biol:47–55Google Scholar
  99. Wild G, West SA (2007) A sex allocation theory for vertebrates: combining local resource competition and condition-dependent allocation. Am Nat 170(5):E112–E128CrossRefPubMedGoogle Scholar
  100. Zijlstra M, Daan S, Bruinenberg-Rinsma J (1992) Seasonal variation in the sex ratio of marsh harrier Circus aeruginosus broods. Funct Ecol:553–559Google Scholar

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© Springer International Publishing AG 2018

Authors and Affiliations

  • Kristen J. Navara
    • 1
  1. 1.Department of Poultry ScienceThe University of GeorgiaAthensUSA

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