Behavioral Ecology and Sociobiology

, Volume 58, Issue 4, pp 407–413 | Cite as

Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection

  • Thomas W. Pike
Original Article


A number of recent reports have documented offspring sex ratio biases in birds. However, to date the potential mechanisms that have been put forward to explain the proximate basis for these deviations are entirely speculative. Using a captive population of domestic pigeons (Columba livia domestica), I tested the hypothesis that mothers in relatively poor physical condition should overproduce daughters by manipulating maternal body condition around the time of egg laying by continuous egg removal and differing feeding regimes. During treatment, females were fed a controlled quantity of food. This, combined with the high energetic costs of repeated egg production caused a significant reduction in maternal body weight. In contrast, during control when food was available ad libitum, maternal body weight did not decline, despite repeated egg production. No significant deviation from parity was evident in the sex ratio of either the first or second eggs during control, whereas during treatment a significant female bias was evident in not only the first egg, but also in the second egg. The absence of single-egg clutches, the rarity of infertile eggs and the lack of laying delays between eggs strongly suggests that the mechanism of sex ratio adjustment in pigeons occurs prior to ovulation. The highly skewed sex-distribution within the two-egg clutches and the unexpectedly large amount of variation in the yolk weight of eggs produced during treatment (but not control) are consistent with the expectations of pre-ovulatory selective resorption of ‘wrong’ sex ovarian follicles.


Selective resorption Primary sex ratio Pre-ovulation manipulation 



I am grateful to the Biotechnology and Biological Sciences Research Council for financial support and to Marion Petrie and two anonymous referees for valuable comments which greatly improved the manuscript. The experiment outlined here complies with the current laws of the United Kingdom


  1. Abs M (1983) The physiology and behaviour of the pigeon. Academic Press, LondonGoogle Scholar
  2. Ankney CD (1982) Sex ratio varies with egg sequence in lesser snow geese. Auk 99:662–666Google Scholar
  3. Arnold KE, Griffith SC, Goldizen AW (2001) Sex-biased hatching sequences in the cooperatively breeding Noisy Miner. J Avian Biol 32:219–223Google Scholar
  4. Arnold KE, Orr KJ, Griffiths R (2003) Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs. Mol Ecol 12:3451–3458Google 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 295:316–318Google Scholar
  6. Bradbury RB, Blakey JK (1998) Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata. Proc R Soc Lond B 265:895–899Google Scholar
  7. Bruford MW, Hanotte O, Brookfield JFY, Burke T (1998) Multilocus and single-locus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach, 2nd edn. IRL Press, Oxford, pp 287–336Google Scholar
  8. Charnov EL (1982) Parent-offspring conflict over reproductive effort. Am Nat 119:736–737Google Scholar
  9. 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 107:13–18Google Scholar
  10. Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals: can the hypotheses be disentangled? In: Hardy I (ed) The sex ratio handbook. Cambridge University Press, CambridgeGoogle Scholar
  11. Edmunds SR, Ankney CD (1987) Sex ratios of hatchling mourning doves. Can J Zool 65:871–874Google Scholar
  12. Emlen ST (1997) When mothers prefer daughters over sons. Trends Ecol Evol 12:291–292Google Scholar
  13. Ewen JG, Cassey P, Moller AP (2004) Facultative primary sex ration variation: a lack of evidence in birds? Proc R Soc Lond B 271:1277–1282Google Scholar
  14. Fiala KL (1981) Sex ratio constancy in the red-winged blackbird. Evolution 35:898–910Google Scholar
  15. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121Google Scholar
  16. Griffiths R, Double C, Orr K, Dawson R (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075Google Scholar
  17. Hanson HC, Kosack CW (1963) The mourning dove in Illinois III. Dept. Conserv Tech Bull No. 4Google Scholar
  18. Hawkins P, Morton DB, Cameron D, Cuthill I, Francis R, Freire R, Gosler A, Healy S, Hudson A, Inglis I, Kirkwood J, Lawton M, Monaghan P, Sherwin C, Townsend P (2001) Laboratory birds: refinements in husbandry and procedures. Lab Anim-UK 35:S1–S163Google Scholar
  19. Heinsohn R, Legge S, Barry S (1997) Extreme bias in sex allocation in Eclectus parrots. Proc R Soc Lond B 264:1325–1329Google Scholar
  20. Houston DC, Jones PJ, Sibley RM (1983) The effect of female body condition on egg-laying in lesser back backed gulls Larus fuscus. J Zool 200:509–520Google Scholar
  21. Johnson AL, van Tienhoven A (1980) Plasma concentrations of six steroids and LH during the ovulatory cycle of the hen, Gallus domesticus. Biol Reprod 23:386–393Google Scholar
  22. Johnston RF, Janiga M (1995) Feral pigeons. Oxford University Press, New YorkGoogle Scholar
  23. 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 268:2175–2179Google Scholar
  24. Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56:155–164Google Scholar
  25. King JR (1973) Energetics of reproduction in birds. In: Farner DS (ed) Breeding biology of birds. National Academy of Sciences, Washington, D.C., pp 78–106Google Scholar
  26. Komdeur J, Daan S, Tinbergen J, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385:522–525Google Scholar
  27. Komduer J, Magrath MJL, Krackow S (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proc R Soc Lond B 269:1067–1072Google Scholar
  28. Kotov AA (1978) Data on the ecology and behaviour of the rock dove in the Southern Urals and Western Siberia. Byull Moskovsk O-va Isp Prirodi Otd Biol, 83:71–80Google Scholar
  29. Krackow S (1995) Potential mechanism for sex ratio adjustment in mammals and birds. Biol Rev 70:225–241Google Scholar
  30. Krackow S (1999) Avian sex ratio distortions: The myth of maternal control. In: Adams N, Slotow R (eds) 22nd International Ornithological Congress, vol. 1. Bird Life South Africa, Durban, pp 425–433Google Scholar
  31. Levi WM (1945) The pigeon. Bryan, Columbia, S.C.Google Scholar
  32. Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc R Soc Lond B 265:1731–1735Google Scholar
  33. MacGregor WC (1958) Non-unisexual broods in the mourning dove. J Wildl Manage 22:103Google Scholar
  34. Nager RG, Monaghan P, Griffiths R, Houston DC, Dawson R (1999) Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci USA 96:570–573Google Scholar
  35. Oddie K (1998) Sex discrimination before birth. Trends Ecol Evol 13:130–131Google Scholar
  36. Pen I, Weissing FJ (2000) Optimal sex allocation: steps towards a mechanistic theory. In: Hardy I (ed) The sex ratio handbook. Cambridge University Press, Cambridge, pp 59–69Google Scholar
  37. Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Sex differences in avian yolk hormone levels. Nature 412:489Google Scholar
  38. Pike TW, Petrie M (2003) Potential mechanisms of avian sex manipulation. Biol Rev 78:553–574Google Scholar
  39. Riddle O (1917) The control of sex ratio. J Wash Acad Sci 7:319–356Google Scholar
  40. Sheldon BC, Andersson S, Griffith SC, Ornborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877Google Scholar
  41. Sturkie PD (1986) Avian Physiology. Springer, Berlin Heildelberg New YorkGoogle Scholar
  42. Teather KL (1987) Intersexual differences in food consumption by hand-reared great-tailed grackle (Quiscalus mexicanus) nestlings. Auk 104:635–639Google Scholar
  43. Teather KL, Weatherhead PJ (1988) Sex-specific energy-requirements of great-tailed grackle (Quiscalus mexicanus) nestlings. J Anim Ecol 57:659–668Google Scholar
  44. Veasey JS, Houston DC, Metcalfe NB (2001) A hidden cost of reproduction: the trade-off between clutch size and escape take-off speed in female zebra finches. J Anim Ecol 70:20–24Google Scholar
  45. Whittingham LA, Dunn PO (2000) Offspring sex ratios in tree swallows: females in better condition produce more sons. Mol Ecol 9:1123–1129Google Scholar
  46. Williams TD (1999) Parental and first generation effects of exogeneous 17β-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata). Horm Behav 35:135–143Google Scholar
  47. Wood-Gush DGM, Gilbert AB (1970) The rate of egg loss through internal laying. Br Poult Sci 11:161–163Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Evolution and Behaviour Research Group, School of BiologyUniversity of Newcastle upon TyneNewcastle upon TyneUK
  2. 2.Institute of Biomedical and Life Sciences, Division of Environmental and Evolutionary BiologyUniversity of GlasgowGlasgowUK

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