Advertisement

Oecologia

, Volume 156, Issue 2, pp 441–453 | Cite as

Male-biased brood sex ratio depresses average phenotypic quality of barn swallow nestlings under experimentally harsh conditions

  • Nicola Saino
  • Rosa Mary de Ayala
  • Roberta Martinelli
  • Giuseppe Boncoraglio
Behavioral Ecology - Original Paper

Abstract

Sex allocation strategies are believed to evolve in response to variation in fitness costs and benefits arising from the production of either sex and can be influenced by the differential susceptibility of sons and daughters to environmental conditions. We tested the effects of manipulating brood size and the sex ratio of the nestmates and the effect of sex on the phenotypic quality of individual barn swallow (Hirundo rustica) nestlings. Brood enlargement, which results in harsh rearing conditions, negatively affected the morphology and immunity of the nestlings. However, the negative consequences of brood enlargement were more marked among male than female offspring. In enlarged but not reduced broods, high proportions of male nestmates resulted in lowered individual body mass, body condition and feather growth. Thus, the consequences of a harsh environment on individual nestlings differed between the sexes and depended on the sex ratio among the other nestlings in the brood. The evolution of sex allocation strategies may therefore depend on the sex of individual nestlings but also on an interaction between environment and progeny sex ratio.

Keywords

Body size Brood size Growth Immunity Sex Sex allocation Sex ratio 

Notes

Acknowledgment

A FPI Grant (Research Training Program) from the Spanish Ministry of Education and Science supported R.M.d.A.

References

  1. Alatalo RV, Lundberg A (1986) Heritability and selection on tarsus length in the pied flycatcher (Ficedula hypoleuca). Evolution 40:474–483CrossRefGoogle Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Badyaev AV (2002) Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol 17:369–378CrossRefGoogle Scholar
  4. Boncoraglio G, Martinelli R, Saino N (2008) Sex-related asymmetry in competitive ability in sexually monomorphic barn swallow nestlings. Behav Ecol Sociobiol.  doi 10.1007/s00265-007-0498-8
  5. Bortolotti GR (1986) Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am Nat 127:495–507CrossRefGoogle Scholar
  6. 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 137:140–147PubMedCrossRefGoogle Scholar
  7. 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
  8. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  9. Crawley MJ (1993) GLIM for ecologists. Blackwell Scientific, OxfordGoogle Scholar
  10. de Ayala RM, Martinelli R, Saino N (2006) Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica). Behav Ecol Sociobiol 60:619–630CrossRefGoogle Scholar
  11. 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
  12. Ferrari RP, Martinelli R, Saino N (2006) Differential effects of egg albumen content on barn swallow nestlings in relation to hatch order. J Evol Biol 19:981–993PubMedCrossRefGoogle Scholar
  13. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  14. Godfray HCJ (1995a) Signalling of need between parents and young: parent–offspring conflict and sibling rivalry. Am Nat 146:1–24CrossRefGoogle Scholar
  15. Godfray HCJ (1995b) Evolutionary theory of parent–offspring conflict. Nature 376:133–138PubMedCrossRefGoogle Scholar
  16. Gorman HE, Nager RG (2004) Prenatal developmental conditions have long-term effects on offspring fecundity. Proc R Soc Lond B 271:1923–1928CrossRefGoogle Scholar
  17. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  18. 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
  19. 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
  20. Krijgsveld KL, Dijkstra C, Visser GH, Daan S (1998) Energy requirements for growth in relation to sexual size dimorphism in marsh harrier Circus aeruginosus nestlings. Physiol Zool 71:693–702PubMedGoogle Scholar
  21. Lessells CM (1991) The evolution of life histories. In: Krebs JR, Davies N (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell Scientific, Oxford, pp 32–68Google Scholar
  22. Lessells CM, Oddie KR, Mateman AC (1998) Parental behaviour is unrelated to experimentally manipulated great tit brood sex ratio. Anim Behav 56:385–393PubMedCrossRefGoogle Scholar
  23. Lochmiller RL, Vestey MR, Boren JC (1993) Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. Auk 110:503–510Google Scholar
  24. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  25. Merilä J, Fry JD (1998) Genetic variation and causes of genotype-environment interaction in body size of blue tits. Genetics 148:1233–1244PubMedGoogle Scholar
  26. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, OxfordGoogle Scholar
  27. Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
  28. Moreno J, Merino S, Sanz JJ, Arriero E, Morales J, Tomas J (2005) Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the pied flycatcher (Ficedula hypoleuca). J Avian Biol 36:251–260CrossRefGoogle Scholar
  29. Oddie KR (2000) Size matters: competition between male and female great tit offspring. J Anim Ecol 69:903–912CrossRefGoogle Scholar
  30. Partridge L (1989) Lifetime reproductive success and life-history evolution. In: Newton I (ed) Lifetime reproduction in birds. Academic Press, London, pp 421–440Google Scholar
  31. Pettifor RA, Perrins CM, McCleery RH (2001) The individual optimization of fitness: variation in reproductive output including clutch size, mean nestling mass and offspring recruitment, in manipulated broods of great tits Parus major. J Anim Ecol 70:62–79CrossRefGoogle Scholar
  32. Pike TW, Petrie M (2005) Offspring sex ratio is related to paternal train elaboration and yolk corticosterone in peafowl. Biol Lett 1:204–207PubMedCrossRefGoogle Scholar
  33. Potti J, Merino S (1996) Parasites and the ontogeny of sexual size dimorphism in a passerine bird. Proc R Soc Lond B 263:9–12CrossRefGoogle Scholar
  34. Råberg L, Stjernman M, Nilsson JA (2005) Sex and environmental sensitivity in blue tit nestlings. Oecologia 145:496–503PubMedCrossRefGoogle Scholar
  35. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, LondonGoogle Scholar
  36. Rubolini D, Romano M, Bonisoli Alquati A, Saino N (2006) Early maternal, genetic and environmental components of antioxidant protection, morphology and immunity of yellow-legged gull (Larus michahellis) chicks. J Evol Biol 19:1571–1584PubMedCrossRefGoogle Scholar
  37. Rutstein AN, Slater PJB, Graves JA (2004) Diet quality and resource allocation in the zebra finch. Proc R Soc Lond B 271:S286–S289CrossRefGoogle Scholar
  38. Saino N, Calza S, Møller AP (1997) Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66:827–836CrossRefGoogle Scholar
  39. Saino N, Calza S, Ninni P, Møller AP (1999a) Barn swallows trade survival against offspring condition and immunocompetence. J Anim Ecol 68:999–1009CrossRefGoogle Scholar
  40. Saino N, de Ayala RM, Boncoraglio G, Martinelli R (2007) Sex difference in mouth coloration and begging calls of barn swallow nestlings. Anim Behav doi:  10.1016/j.anbehav.2007.09.011
  41. Saino N, Ellegren H, Møller AP (1999b) No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows. Mol Ecol 8:399–406CrossRefGoogle Scholar
  42. Saino N, Ninni P, Incagli M, Calza S, Sacchi R, Møller AP (2000) Begging and parental care in relation to offspring need and condition in the barn swallow (Hirundo rustica). Am Nat 156:637–649CrossRefGoogle Scholar
  43. Saino N, Ferrari RP, Romano M, Ambrosini R, Møller AP (2002a) Ectoparasites and the cost of reproduction in the barn swallow (Hirundo rustica). Oecologia 133:139–145CrossRefGoogle Scholar
  44. Saino N, Ambrosini R, Martinelli R, Møller AP (2002b) Mate fidelity, senescence in breeding performance, and reproductive trade-offs in the barn swallow. J Anim Ecol 71:309–319CrossRefGoogle Scholar
  45. Saino N, Ambrosini R, Martinelli R, Calza S, Møller AP, Pilastro A (2002c) Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow. Mol Ecol 11:1533–1544PubMedCrossRefGoogle Scholar
  46. Saino N, Suffritti C, Martinelli R, Rubolini D, Møller AP (2003a) Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica). Behav Ecol 14:318–325CrossRefGoogle Scholar
  47. Saino N, Galeotti P, Sacchi R, Boncoraglio G, Martinelli R, Møller AP (2003b) Sex differences in begging vocalizations of nestling barn swallows, Hirundo rustica. Anim Behav 66:1003–1010 CrossRefGoogle Scholar
  48. Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2005) Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring. J Exp Zool 303A:998–1006CrossRefGoogle Scholar
  49. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer, SunderlandGoogle Scholar
  50. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  51. Teather KL, Weatherhead PJ (1998) Sex-specific energy requirements of great tailed grackle (Quiscalus mexicanus) nestlings. J Anim Ecol 57:659–668Google Scholar
  52. Tinbergen JM (2005) Biased estimates of fitness consequences of brood size manipulation through correlated effects on natal dispersal. J Anim Ecol 74:1112–1120CrossRefGoogle Scholar
  53. Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–265Google Scholar
  54. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary sex-ratio of offspring. Science 179:90–92PubMedCrossRefGoogle Scholar
  55. Tschirren B, Fitze PS, Richner H (2003) Sexual dimorphism in susceptibility to parasites and cell-mediated immunity in great tit nestlings. J Anim Ecol 72:839–845CrossRefGoogle Scholar
  56. Uller T (2006) Sex-specific sibling interactions and offspring fitness in vertebrates: patterns and implications for maternal sex ratios. Biol Rev 81:207–217PubMedCrossRefGoogle Scholar
  57. West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688PubMedCrossRefGoogle Scholar
  58. 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

© Springer-Verlag 2008

Authors and Affiliations

  • Nicola Saino
    • 1
  • Rosa Mary de Ayala
    • 2
    • 3
  • Roberta Martinelli
    • 1
  • Giuseppe Boncoraglio
    • 1
  1. 1.Dipartimento di BiologiaUniversità degli Studi di MilanoMilanItaly
  2. 2.Estación Experimental de Zonas ÁridasConsejo Superior de Investigaciones CientíficasAlmeríaSpain
  3. 3.Centre for Ecological and Evolutionary Synthesis (CEES)Department of Biology, University of OsloBlindern, OsloNorway

Personalised recommendations