Natural history miscellany: Temporal but not spatial environmental variation drives adaptive offspring sex allocation in a plural cooperative breeder

American Naturalist

Volumn 170, Issue 1, 2007, Pages 155-165

  Rubenstein, Dustin R ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cooperative breeding; Environmental unpredictability; Maternal condition; Sex allocation; Spatiotemporal environmental variation; Trivers Willard

Indexed keywords

COOPERATIVE BREEDING; FITNESS; MATERNAL CARE; PASSERINE; REPRODUCTIVE SUCCESS; SEX ALLOCATION; SPATIAL VARIATION;

AVES; LAMPROTORNIS SUPERBUS; STURNIDAE;

ADAPTATION; ANIMAL; ARTICLE; BIOLOGICAL MODEL; BREEDING; COOPERATION; ENVIRONMENT; FEMALE; GENDER AND SEX; MALE; NESTING; PHYSIOLOGY; SEX DIFFERENCE; SEX RATIO; STARLING;

ADAPTATION, BIOLOGICAL; ANIMALS; BREEDING; COOPERATIVE BEHAVIOR; ENVIRONMENT; FEMALE; MALE; MODELS, BIOLOGICAL; NESTING BEHAVIOR; SEX DETERMINATION (GENETICS); SEX FACTORS; SEX RATIO; STARLINGS;

EID: 34250811923     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/518671     Document Type: Article

References (65)

1. Appleby, B. M., S. J. Petty, J. K. Blakey, P. Rainey, and D. W. MacDonald. 1997. Does variation of sex ratio enhance reproductive success of offspring in tawny owls (Strix aluco)?. Proceedings of the Royal Society B: Biological Sciences 264:1111-1116.
2. Augustine, D. J. 2003. Long-term, livestock-mediated redistribution of nitrogen and phosphorus in an East African savanna. Journal of Applied Ecology 40:137-149.
3. Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2:349-368.
4. Bradbury, R. R., and J. K. Blakey. 1998. Diet, maternal condition, and offspring sex ratio in the zebra finch, Poephila guttata. Proceedings of the Royal Society B: Biological Sciences 265:895-899.
5. Brown, J. L. 1987. Helping and communal breeding in birds: ecology and evolution. Princeton University Press, Princeton, NJ.
6. Buchanan, K. L., K. A. Spencer, A. R. Goldsmith, and C. K. Catchpole. 2003. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proceedings of the Royal Society B: Biological Sciences 270:1149-1156.
7. Cameron, E. Z., and W. L. Linklater. 2002. Sex bias in studies of sex bias: the value of daughters to mothers in poor condition. Animal Behaviour 63:F5-F8.
8. Charnov, E. L. 1982. The theory of sex allocation. Princeton University Press, Princeton, NJ.
9. Clark, A. B. 1978. Sex ratio and local resource competition in a prosimian primate. Science 201:163-165.
10. Clutton-Brock, T. H., and G. R. Iason. 1986. Sex ratio variation in mammals. Quarterly Review of Biology 61:339-374.
11. Cockburn, A. 1998. Evolution of helping behaviour in cooperatively breeding birds. Annual Review of Ecology and Systematics 29:141-177.
12. Covas, R., C. Doutrelant, and M. A. du Plessis. 2004. Experimental evidence of a link between breeding condition and the decision to breed or help in a colonial cooperative bird. Proceedings of the Royal Society B: Biological Sciences 271:827-832.
13. Cuthill, I. C., S. A. Maddocks, C. V. Weall, and E. K. M. Jones. 2000. Body mass regulation in response to changes in feeding predictability and overnight energy expenditure. Behavioral Ecology 11:189-195.
14. Dickinson, J. L. 2004. Facultative sex ratio adjustment by western bluebird mothers with stay-at-home helpers at the nest. Animal Behaviour 68:373-380.
15. Doutrelant, C., R. Covas, A. Caizergues, and M. du Plessis. 2004. Unexpected sex ratio adjustment in a colonial cooperative bird: pairs with helpers produce more of the helping sex whereas pairs without helpers do not. Behavioral Ecology and Sociobiology 56:149-154.
16. du Plessis, M. A., W. R. Siegfried, and A. J. Armstrong. 1995. Ecological and life-history correlates of cooperative breeding in South African birds. Oecologia (Berlin) 102:180-188.
17. Emlen, S. T. 1982. The evolution of helping. I. An ecological constraints model. American Naturalist 119:29-39.
18. _. 1997. When mothers prefer daughters over sons. Trends in Ecology & Evolution 12:291-292.
19. Emlen, S. T., J. M. Emlen, and S. A. Levin. 1986. Sex-ratio selection in species with helpers-at-the-nest. American Naturalist 127:1-8.
20. Feare, C., and A. Craig. 1999. Starlings and mynas. Princeton University Press, Princeton, NJ.
21. Fisher, R. A. 1930. The genetical theory of natural selection. Clarendon, Oxford.
22. Frank, S. A. 1990. Sex allocation theory for birds and mammals. Annual Review of Ecology and Systematics 21:13-55.
23. Fry, C. H., S. Keith, and E. K. Urban. 2000. The birds of Africa. Academic Press, San Diego, CA.
24. Gowaty, P. A., and M. R. Lennartz. 1985. Sex ratios of nestling and fledgling red-cockaded woodpeckers (Picoides borealis) favors males. American Naturalist 126:347-353.
25. Greenwood, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28:1140-1162.
26. Griffin, A. S., B. C. Sheldon, and S. A. West. 2005. Cooperative breeders adjust offspring sex ratios to produce helpful helpers. American Naturalist 166:628-632.
27. Griffiths, R., M. C. Double, K. Orr, and R. J. G. Dawson. 1998. A DNA test to sex most birds. Molecular Ecology 7:1071-1075.
28. Hamilton, W. D. 1967. Extraordinary sex ratios. Science 156:477-488.
29. Hasselquist, D., and B. Kempenaers. 2002. Parental care and adaptive brood sex ratio manipulation in birds. Philosophical Transactions of the Royal Society B: Biological Sciences 357:363-372.
30. Hauber, M. E., and E. A. Lacey. 2005. Bateman's principle in cooperatively breeding vertebrates: the effects of non-breeding alloparents on variability in female and male reproductive success. Integrative and Comparative Biology 45:903-914.
31. Jacobs, J. D., and J. C. Wingfield. 2000. Endocrine control of life-cycle stages: a constraint on response to the environment? Condor 102:35-51.
32. Julliard, R. 2000. Sex-specific dispersal in spatially varying environments leads to habitat-dependent evolutionary stable offspring sex ratios. Behavioral Ecology 4:421-428.
33. Kilner, R. 1998. Primary and secondary sex ratio manipulation by zebra finches. Animal Behaviour 56:155-164.
34. Koenig, W. D., and E A. Pitelka. 1981. Ecological factors and kin selection in the evolution of cooperative breeding in birds. Pages 261-280 in R. D. Alexander and D. W. Tinkle, eds. Natural selection and social behavior. Chiron, New York.
35. Koenig, W. D., F. A. Pitelka, W. J. Carmen, R. L. Mumme, and M. T. Stanback. 1992. The evolution of delayed dispersal in cooperative breeders. Quarterly Review of Biology 67:111-150.
36. Komdeur, J. 1996a. Facultative sex ratio bias in the offspring of Seychelles warblers. Proceedings of the Royal Society B: Biological Sciences 263:661-666.
37. _. 1996b. Influence of age on reproductive performance in the Seychelles warbler. Behavioral Ecology 7:417-425.
38. _. 1996c. Seasonal timing of reproduction in a tropical bird, the Seychelles warbler: a field experiment using translocation. Journal of Biological Rhythms 11:333-346.
39. _. 1998. Long-term fitness benefits of egg sex modification by the Seychelles warbler. Ecology Letters 1:56-62.
40. _. 2003. Daughters on request: about helpers and egg sexes in the Seychelles warbler. Proceedings of the Royal Society B: Biological Sciences 270:3-11.
41. _. 2004. Sex-ratio manipulation. Pages 102-116 in W. D. Koenig and J. Dickinson, eds. Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge.
42. Komdeur, J., S. Daan, J. Tinbergen, and C. Mateman. 1997. Extreme adaptive modification in sex ratio of the Seychelles warbler's egg. Nature 385:522-525.
43. Lessels, C. M., and M. I. Avery. 1987. Sex ratio selection in species with helpers at the nest: some extensions of the repayment model. American Naturalist 129:610-620.
44. Love, O. P., E. H. Chin, K. E. Wynne-Edwards, and T. D. Williams. 2005. Stress hormones: a link between maternal condition and sex-biased reproductive investment. American Naturalist 166:751-766.
45. Millon, A., and V. Bretagnolle. 2005. Nonlinear and population-specific offspring sex ratios in relation to high variation in prey abundance. Oikos 108:535-543.
46. Nager, R. G., P. Monaghan, and A. I. Houston. 2000. Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus). Behavioral Ecology and Sociobiology 48:452-457.
47. Pen, I., and F. J. Weissing. 2000. Sex-ratio optimization with helpers at the nest. Proceedings of the Royal Society B: Biological Sciences 267:539-543.
48. Pike, T. W., and M. Petrie 2006. Experimental evidence that corticosterone affects offspring sex ratios in quail. Proceedings of the Royal Society B: Biological Sciences 273:1093-1098.
49. Rosenfeld, C. S., and R. M. Roberts. 2004. Maternal diet and other factors affecting offspring sex ratio: a review. Biology of Reproduction 71:1063-1070.
50. Rubenstein, D. R. 2006. The evolution of the social and mating systems of the plural cooperatively breeding superb starling, Lamprotornis superbus. PhD diss. Cornell University, Ithaca, NY.
51. _. 2007. Stress hormones and sociality: integrating social and environmental stressors. Proceedings of the Royal Society B: Biological Sciences 274:967-975.
52. _. Forthcoming a. Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proceedings of the Royal Society B: Biological Sciences.
53. _. Forthcoming b. Territory quality drives intraspecific patterns of extrapair paternity. Behavioral Ecology.
54. Rutkowska, J., and M. Cichon. 2002. Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Animal Behaviour 64:817-822.
55. Stacey, P. B., and J. D. Ligon. 1991. The benefits-of-philopatry hypothesis for the evolution of cooperative breeding: variation in territory quality and group size effects. American Naturalist 137:831-846.
56. Stauss, M., G. Segelbacher, J. Tomiuk, and L. Bachmann. 2005. Sex ratio of Parus major and P. caeruleus broods depends on parental condition and habitat quality. Oikos 109:367-373.
57. Suorsa, P., H. Helle, E. Huhta, A. Jantti, A. Nikula, and H. Hakkarainen. 2003. Forest fragmentation is associated with primary brood sex ratio in the treecreeper (Certhia familiaris). Proceedings of the Royal Society B: Biological Sciences 270:2215-2222.
58. Trivers, R. L., and D. E. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90-92.
59. Ward, D., D. Saltz, and B. T. Ngairorue. 2004. Spatio-temporal rainfall variation and stock management in arid Namibia. Journal of Range Management 57:130-140.
60. Weatherhead, P. J., and P. T. Boag. 1997. Genetic estimates of annual and lifetime reproductive success in male red-winged blackbirds. Ecology 78:884-896.
61. Whittingham, L. A., and P. O. Dunn. 2000. Offspring sex ratios in tree swallows: females in better condition produce more sons. Molecular Ecology 9:1123-1129.
62. Wiebe, K. L., and G. R. Bortolotti. 1992. Facultative sex ratio manipulation in American kestrels. Behavioral Ecology and Sociobiology 30:379-386.
63. Wilson, K., and I. C. W. Hardy. 2002. Statistical analysis of sex ratios: an introduction. Pages 48-92 in I. C. W. Hardy, ed. Sex ratios: concepts and research methods. Cambridge University Press, Cambridge.
64. Witter, M. S., J. P. Swaddle, and I. C. Cuthill. 1995. Periodic food availability and strategic regulation of body mass in the European starling, Sturnus vulgaris. Functional Ecology 9:568-574.
65. Zann, R., and D. Runciman. 2003. Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations. Behavioral Ecology and Sociobiology 54:294-302.