Intraclutch differences in egg characteristics mitigate the consequences of age-related hierarchies in a wild passerine

Evolution

Volumn 67, Issue 9, 2013, Pages 2688-2700

  Hadfield, Jarrod D ^a,b   Heap, Elizabeth A ^b   Bayer, Florian ^b   Mittell, Elizabeth A ^b   Crouch, Nicholas M A ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Cyanistes caeruleus; Development; Eggs; Maternal effects; Quantitative genetics; Selection

Indexed keywords

AGE STRUCTURE; BIOLOGICAL CHARACTERISTICS; CLUTCH SIZE; EGG DEVELOPMENT; EXPERIMENTAL STUDY; GROWTH RATE; HIERARCHICAL SYSTEM; PASSERINE; WILD POPULATION;

CYANISTES CAERULEUS; PASSERI; PASSERIFORMES;

AGE; ANIMAL; ANIMAL EMBRYO; ARTICLE; CYANISTES CAERULEUS; DEVELOPMENT; EGG; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HISTOLOGY; MATERNAL EFFECTS; PHYSIOLOGY; POPULATION; QUANTITATIVE GENETICS; REPRODUCTION; SELECTION; SONGBIRD;

CYANISTES CAERULEUS; DEVELOPMENT; EGGS; MATERNAL EFFECTS; QUANTITATIVE GENETICS; SELECTION;

AGE FACTORS; ANIMALS; EMBRYO, NONMAMMALIAN; GENETIC VARIATION; PASSERIFORMES; POPULATION; REPRODUCTION; SELECTION, GENETIC;

EID: 84883555747     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12143     Document Type: Article

References (56)

1. Badyaev, A. V., M. L. Beck, G. E. Hill, and L. A. Whittingham 2003. The evolution of sexual size dimorphism in the house finch. V. maternal effects. Evolution 57:384-396.
2. Badyaev, A. V., G. E. Hill, M. L. Beck, A. A. Dervan, R. A. Duckworth, K. J. McGraw, P. M. Nolan, and L. A. Whittingham, 2002. Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295:316-318.
3. Butler, D., B. R. Cullis, A. R. Gilmour, and B. J. Gogel, 2007. Analysis of mixed models for S-language environments: ASReml-R reference manual. Queensland DPI, Brisbane, Australia. Available at http://www.vsni.co.uk/resources/doc/asreml-R.pdf.
4. Clark, A. B., and D. S. Wilson 1981. Avian breeding adaptations-hatching asynchrony, brood reduction, and nest failure. Q. Rev. Biol. 56:253-277.
5. Cresswell, W., and R. McCleery 2003. How great tits maintain synchronization of their hatch date with food supply in response to long-term variability in temperature. J. Anim. Ecol. 72:356-366.
6. de Villemereuil, P., O. Gimenez, and D. Blandine 2012. Estimating heritability of continuous and binary traits in wild populations when individuals share or not environmental effects: which method to use? Methods Ecol. Evol. 4:260-275.
7. Drent, R. 1975. Incubation. Pp. 333-420, in D. S. Farner and J. R. King, eds. Avian biology. Vol. 5. Academic Press, New York.
8. Ganeshaiah, K. N., and R. U. Shaanker 1988. Seed abortion in wind-dispersed pods of Dalbergia sissoo-maternal regulation or sibling rivalry. Oecologia 77:135-139.
9. Gelman, A. 2006. Prior distributions for variance parameters in hierarchical models. Bayesian Anal. 1:515-533.
10. Gelman, A., A. Jakulin, M. G. Pittau, and Y. S. Su 2008. A weakly informative default prior distribution for logistic and other regression models. Ann. Appl. Stat. 2:1360-1383.
11. Gibb, J. 1950. The breeding biology of the great and blue titmice. Ibis 92:501-539.
12. Gibson, M. A., and E. Gurmu 2010. Land inheritance establishes sibling competition for marriage and reproduction in rural ethiopia. Proc. Natl. Acad. Sci. U.S.A. 108:2200-2204.
13. Gil, D. 2003. Golden eggs: maternal manipulation of offspring phenotype by egg androgen in birds. Ardeola 50:281-294.
14. Gilmour, A. R., B. J. Gogel, B. R. Cullis, S. J. Welham, and R. Thompson 2002. ASReml user guide release 1.0. VSN International Ltd, Hemel Hempstead, U.K. Available at http://www.VSN-Intl.com.
15. Groothuis, T. G. G., W. Muller, N. von Engelhardt, C. Carere, and C. Eising 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci. Biobehav. Rev. 29:329-352.
16. Groothuis, T. G. G., and H. Schwabl 2008. Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Proc. R. Soc. Lond. B Biol. Sci. 363:1647-1661.
17. Hadfield, J., E. A. Heap, F. Bayer, E. A. Mittell, and C. M. A. 2013. Disentangling genetic and prenatal sources of familial resemblance across ontogeny in a wild passerine. Evolution 67:2701-2713.
18. Hadfield, J. D. 2010. MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33:1-22.
19. Hadfield, J. D., D. S. Richardson, and T. Burke 2006. Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Mol. Ecol. 15:3715-3731.
20. Heitjan, D. F. 1993. Ignorability and coarse data-some biomedical examples. Biometrics 49:1099-1109.
21. Heitjan, D. F., and D. B. Rubin 1991. Ignorability and coarse data. Ann. Stat. 19:2244-2253.
22. Henderson, C. R. 1950. Estimation of genetic parameters. Ann. Math. Stat. 21:309-310.
23. Henderson, C. R. 1976. Simple method for computing inverse of a numerator relationship matrix used in prediction of breeding values. Biometrics 32:69-83.
24. Howe, H. F. 1976. Egg size, hatching asynchrony, sex, and brood reduction in common grackle. Ecology 57:1195-1207.
25. Hussell, D. J. T. 1972. Factors affecting clutch size in arctic passerines. Ecol. Monogr. 42:317-364.
26. Kingma, S. A., J. Komdeur, O. Vedder, N. von Engelhardt, P. Korsten, and T. G. G. Groothuis 2009. Manipulation of male attractiveness induces rapid changes in avian maternal yolk androgen deposition. Behav. Ecol. 20:172-179.
27. Lack, D. 1947. The significance of clutch-size. Ibis 89:302-352.
28. Magrath, R. D. 1990. Hatching asynchrony in altricial birds. Biol. Rev. Camb. Philos. Soc. 65:587-622.
29. Mainwaring, M. C., M. Dickens, and I. R. Hartley 2010. Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird. J. Evol. Biol. 23:1302-1311.
30. Mock, D. W., H. Drummond, and C. H. Stinson 1990. Avian siblicide. Am. Sci. 78:438-449.
31. Mock, D. W., and G. A. Parker 1997. The evolution of sibling rivalry. Oxford Univ. Press, Oxford, U.K.
32. Muck, C., and R. G. Nager 2006. The effect of laying and hatching order on the timing and asynchrony of hatching. Anim. Behav. 71:885-892.
33. Muller, M., and T. G. G. Groothuis 2013. Within-clutch variation in yolk testosterone as an adaptive maternal effect to modulate avian sibling competition: evidence from a comparative study. Am. Nat. 181:125-136.
34. Muller, W., C. M. Lessells, P. Korsten, and N. von Engelhardt 2007. Manipulative signals in family conflict? on the function of maternal yolk hormones in birds. Am. Nat. 169:E84-E96.
35. Nilsson, J. A., and E. Svensson 1993. Energy constraints and ultimate decisions during egg-laying in the blue tit. Ecology 74:244-251.
36. Nitsch, A., F. Faurie, and V. Lummaa 2013. Are elder siblings helpers or competitors? Antagonistic fitness effects of sibling interactions in humans. Proc. R. Soc. Lond. B Biol. Sci. 280:20122313.
37. Parsons, J. 1975. Asynchronous hatching and chick mortality in herring gull Larus argentatus. Ibis 117:517-520.
38. Perrins, C. M. 1979. British tits. Collins, London, U.K.
39. Pettifor, R. A., C. M. Perrins, and R. H. McCleery 1988. Individual optimization of clutch size in great tits. Nature 336:160-162.
40. Pullen, N. D. 1946. Further notes on the breeding of blue tits. Br. Birds 39:162-167.
41. R Development Core Team. 2012. R: a language and environment for statistical computing. Available at http://www.R-project.org. ISBN 3-900051-07-0.
42. Ramsay, S. L., and D. C. Houston 1997. Nutritional constraints on egg production in the blue tit: a supplementary feeding study. J. Anim. Ecol. 66:649-657.
43. Royle, N. J., P. F. Surai, and I. R. Hartley 2001. Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav. Ecol. 12:381-385.
44. Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. U.S.A. 90:11446-11450.
45. Schwabl, H. 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. A Physiol. 114:271-276.
46. Schwabl, H., D. W. Mock, and J. A. Gieg 1997. A hormonal mechanism for parental favouritism. Nature 386:231-231.
47. Shizuka, D., and B. E. Lyon 2010. Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463:223-226.
48. Slagsvold, T. 1986. Asynchronous versus synchronous hatching in birds - experiments with the pied flycatcher. J. Anim. Ecol. 55:1115-1134.
49. Slagsvold, T., J. Sandvik, G. Rofstad, O. Lorentsen, and M. Husby 1984. On the adaptive value of intraclutch egg-size variation in birds. Auk 101:685-697.
50. Smiseth, P. T., M. P. Scott, and C. Andrews 2011. Hormonal regulation of offspring begging and mediation of parent-offspring conflict. Anim. Behav. 81:507-517.
51. Stoleson, S., and S. Beissinger 1995. Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period? Curr. Ornithol. 12:191-270.
52. Tona, K., F. Bamelis, B. De Ketelaere, V. Bruggeman, V. M. B. Moraes, J. Buyse, O. Onagbesan, and E. Decuypere 2003. Effects of egg storage time on spread of hatch, chick quality, and chick juvenile growth. Poult. Sci. 82:736-741.
53. Uller, T. 2008. Developmental plasticity and the evolution of parental effects. Trends Ecol. Evol. 23:432-438.
54. Uller, T., and I. Pen 2011. A theoretical model of the evolution of maternal effects under parent-offspring conflict. Evolution 65:2075-2084.
55. Wang, J., and A. W. Santure 2009. Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579-1594.
56. Wang, J. L. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166:1963-1979.