Journal of Ornithology

, Volume 149, Issue 4, pp 521–527

Offspring sex ratio in the sequentially polygamous Penduline Tit Remiz pendulinus

  • René E. van Dijk
  • Jan Komdeur
  • Marco van der Velde
  • István Szentirmai
  • Xutong Yang
  • Richard Ffrench-Constant
  • Tamás Székely
Original Article

Abstract

Despite the growing literature on facultative sex-ratio adjustment in chromosomal sex-determining vertebrate taxa (birds, mammals), the consistency of results is often low between studies and species. Here, we investigate the primary and secondary offspring sex ratio of a small passerine bird, the Eurasian Penduline Tit (Remiz pendulinus) in three consecutive years. This species has a uniquely diverse breeding system, in which the male (and/or the female) abandons the nest during egg-laying, and starts a new breeding attempt. This allowed us to test (1) whether patterns of parental care, i.e., male-only care, female-only care or biparental desertion, influence offspring sex ratio, and (2) whether the offspring sex ratio is repeatable between successive clutches of males and females. Using molecular markers to sex 497 offspring in 176 broods, we show that (1) offspring sex ratio does not depend on which parent provides care, and (2) the offspring sex ratio is not repeatable between clutches of a given individual. The overall primary and secondary offspring sex ratio at a population level is not different from parity (54 ± 6% males, and 50 ± 3% (mean ± SE), respectively). We suggest that ecological and phenotypic factors, rather than individual traits of parents, may influence offspring’s sex, and conclude that there is currently no evidence for a facultative adjustment of offspring sex ratio in the Penduline Tit.

Keywords

Parental care Breeding system Remiz pendulinus Repeatability Sex allocation 

References

  1. Badyaev AV, Hill GE, Beck ML (2003) Interaction between maternal effects: onset of incubation and offspring sex ratio in two populations of a passerine bird. Oecologia 135:386–390PubMedGoogle Scholar
  2. Bleeker M, Kingma SA, Szentirmai I, Székely T, Komdeur J (2005) Body condition and clutch desertion in penduline tit Remiz pendulinus. Behaviour 142:1465–1478CrossRefGoogle Scholar
  3. Cassey P, Ewen JG, Møller AP (2006) Revised evidence for facultative sex ratio adjustment in birds: a correction. Proc R Soc Lond B 273:3129–3130CrossRefGoogle Scholar
  4. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  5. Cichoń M, Dubiec A, Stoczko M (2003) Laying order and offspring sex in blue tits Parus caeruleus. J Avian Biol 34:355–359CrossRefGoogle Scholar
  6. Clutton-Brock TH (1986) Sex-ratio variation in birds. Ibis 128:317–329CrossRefGoogle Scholar
  7. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  8. Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals:can the hypotheses be disentangled? In: Hardy I (ed) Sex ratios. Concepts and research methods. Cambridge University Press, Cambridge, pp 266–286Google Scholar
  9. Cramp S, Perrins CM, Brooks DJ (1993) Birds of the Western Palearctic, vol VII. Oxford University Press, OxfordGoogle Scholar
  10. Daan S, Dijkstra C, Weissing FJ (1996) An evolutionary explanation for seasonal trends in avian sex ratios. Behav Ecol 7:426–430CrossRefGoogle Scholar
  11. Dean WRJ (2005) Cape penduline tit Anthoscopus minutus. In: Hockey PAR, Dean WRJ, Ryan PG (eds) Roberts Birds of Southern Africa. John Voelker Bird Book Fund, Cape Town, pp 736–737Google Scholar
  12. 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 60:563–571CrossRefGoogle Scholar
  13. Dijkstra C, Bult A, Bijlsma S, Daan S, Meijer T, Zijlstra M (1990) Brood size manipulations in the kestrel (Falco tinnunculus): effects on offspring and parent survival. J Anim Ecol 59:269–286CrossRefGoogle Scholar
  14. Ewen JG, Cassey P, Møller AP (2004) Facultative primary sex ratio variation; a lack of evidence in birds? Proc R Soc Lond B 271:1277–1282CrossRefGoogle Scholar
  15. Fawcett TW, Kuijper B, Pen I, Weissing FJ (2007) Should attractive males have more sons? Behav Ecol 18:71–80CrossRefGoogle Scholar
  16. Festa-Bianchet M (1996) Offspring sex ratio studies of mammals: does publication depend upon the quality of the research or the direction of the results? Ecoscience 3:42–44Google Scholar
  17. Fiala KL (1980) On estimating the primary sex-ratio from incomplete data. Am Nat 115:442–444CrossRefGoogle Scholar
  18. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  19. Franz D (1988) Das Paarungssystem der Beutelmeise (Remiz pendulinus)—ein Kampf der Geschlechter. J Orn 129:107–111CrossRefGoogle Scholar
  20. Franz D (1991) Mating system and strategy of reproduction in penduline tit (Remiz p. pendulinus). J Orn 132:241–266CrossRefGoogle Scholar
  21. Glutz von Blotzheim UN, Bauer KM (1993) Handbuch der Vögel Mitteleuropas, vol 13/2. Aula, WiesbadenGoogle Scholar
  22. Griffin AS, Sheldon BC, West SA (2005) Cooperative breeders adjust offspring sex ratios to produce helpful helpers. Am Nat 166:628–632PubMedCrossRefGoogle Scholar
  23. Griffiths R, Double M, Orr K, Dawson R (1998) A simple DNA test to sex most birds. Mol Ecol 7:1071–1076PubMedCrossRefGoogle Scholar
  24. Grindstaff JL, Buerkle CA, Casto JM, Nolan V Jr, Ketterson ED (2001) Offspring sex ratio is unrelated to male attractiveness in dark-eyed Juncos (Junco hyemalis). Behav Ecol Sociobiol 50:312–316CrossRefGoogle Scholar
  25. Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488PubMedCrossRefGoogle Scholar
  26. Harper DGC (1994) Some comments on the repeatability of measurements. Ringing Migr 15:84–90Google Scholar
  27. Hasselquist D, Kempenaers B (2002) Parental care and adaptive brood sex ratio manipulation in birds. Philos Trans R Soc Lond B 357:363–372CrossRefGoogle Scholar
  28. Hipkiss T, Hornfeldt B (2004) High interannual variation in the hatching sex ratio of Tengmalm’s Owl broods during a vole cycle. Popul Ecol 46:263–268CrossRefGoogle Scholar
  29. Kempenaers B, Verheyen GR, Dhondt AA (1997) Extrapair paternity in the Blue Tit (Parus caeruleus): female choice, male characteristics, and offspring quality. Behav Ecol 8:481–492CrossRefGoogle Scholar
  30. Kilner R (1998) Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56:155–164PubMedCrossRefGoogle Scholar
  31. Kingma SA, Szentirmai I, Székely T, Bókony V, Bleeker M, Liker A, Komdeur J (2008) Sexual selection and the function of a melanin-based plumage ornament in polygamous penduline tits Remiz pendulinus. Behav Ecol Sociobiol (in press)Google Scholar
  32. Komdeur J, Daan S, Tinbergen JM, Mateman C (1997) Extreme adaptive modification in sex ratio of the Seychelles Warbler’s eggs. Nature 385:522–525CrossRefGoogle Scholar
  33. Komdeur J, Magrath MJL, Krackow S (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler.Proc R Soc Lond B 269:1067–1072CrossRefGoogle Scholar
  34. Komdeur J, Pen I (2002) Adaptive sex allocation in birds: the complexities of linking theory and practice. Philos Trans R Soc Lond B 357:373–380CrossRefGoogle Scholar
  35. Korsten P, Lessells CM, Mateman AC, van der Velde M, Komdeur J (2006) Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits. Behav Ecol 17:539–546CrossRefGoogle Scholar
  36. 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 51:447–454CrossRefGoogle Scholar
  37. Leech DI, Hartley IR, Stewart IRK, Griffith SC, Burke T (2001) No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus). Behav Ecol 12:674–680CrossRefGoogle Scholar
  38. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities—a common mistake. Auk 104:116–121Google Scholar
  39. Minitab 12.2 (2004) Minitab, Pa., USAGoogle Scholar
  40. Oddie KR, Reim C (2002) Egg sex ratio and paternal traits: using within-individual comparisons. Behav Ecol 13:503–510CrossRefGoogle Scholar
  41. 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
  42. Persson O, Öhrström P (1989) A new avian mating system: ambisexual polygamy in the penduline tit (Remiz pendulinus). Ornis Scand 20:105–111CrossRefGoogle Scholar
  43. R Development Core Team (2005) A language and environment for statisticalcomputing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  44. Radford AN, Blakey JK (2000) Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11:294–298CrossRefGoogle Scholar
  45. Resampling Stats™ for Excel (2006) Resampling Stats, Arlington, Va.Google Scholar
  46. Saino N, Ellegren H, Møller AP (1999) No evidence for adjustment of sex allocation in relation to parental ornamentation and paternity in Barn Swallow. Mol Ecol 8:399–406CrossRefGoogle Scholar
  47. Sheldon BC, Andersson S, Griffith SC, Örnborg J, Sendecka J (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877CrossRefGoogle Scholar
  48. Sokal RR, Rohlf FJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New YorkGoogle Scholar
  49. SPSS 12.0.0 (2003) SPSS Inc, 1989–2003.ChicagoGoogle Scholar
  50. Székely T, Cuthill IC, Yezerinac S, Griffiths R, Kis J (2004) Brood sex ratio in the Kentish Plover. Behav Ecol 15:58–62CrossRefGoogle Scholar
  51. Szentirmai I, Komdeur J, Székely T (2005) What makes a nest building male successful? Male behaviour and female care in penduline tits. Behav Ecol 16:994–1000CrossRefGoogle Scholar
  52. Szentirmai I, Székely T, Komdeur J (2007) Sexual conflict over care: antagonistic effect of clutch desertion on reproductive success of male and female penduline tits. J Evol Biol 20:1739–1744PubMedCrossRefGoogle Scholar
  53. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92PubMedCrossRefGoogle Scholar
  54. van Dijk RE, Szentirmai I, Komdeur J, Székely T (2007) Sexual conflict over care in penduline tits: the process of clutch desertion. Ibis 149:530–534CrossRefGoogle Scholar
  55. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–518PubMedGoogle Scholar
  56. West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688PubMedCrossRefGoogle Scholar
  57. West SA, Reece SE, Sheldon BC (2002) Sex ratios. Heredity 88:117–124PubMedCrossRefGoogle Scholar
  58. Westneat DF, Stewart IRK, Halpin Woeste E, Gipson J, Abdulkadir L, Poston JP (2002) Patterns of sex ratio variation in house sparrows. Condor 104:598–609CrossRefGoogle Scholar
  59. Whittingham LA, Dunn PO, Nooker JK (2005) Maternal influences on brood sex ratios: an experimental study in tree swallows. Proc R Soc Lond B 272:1775–1780CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2008

Authors and Affiliations

  • René E. van Dijk
    • 1
    • 2
  • Jan Komdeur
    • 2
  • Marco van der Velde
    • 2
  • István Szentirmai
    • 3
    • 4
  • Xutong Yang
    • 1
  • Richard Ffrench-Constant
    • 1
    • 5
  • Tamás Székely
    • 1
  1. 1.Department of Biology and BiochemistryUniversity of BathBathUK
  2. 2.Animal Ecology Group, Centre for Ecological and Evolutionary StudiesUniversity of GroningenHarenThe Netherlands
  3. 3.Department of EthologyEötvös Loránd UniversityBudapestHungary
  4. 4.Őrsèg National ParkOriszentpeterHungary
  5. 5.Centre for Ecology and ConservationUniversity of ExeterPenrynUK

Personalised recommendations