Selection for rapid embryo development correlates with embryo exposure to maternal androgens among passerine birds

American Naturalist

Volumn 170, Issue 2, 2007, Pages 196-206

  Schwabl, Hubert ^a   Palacios, Maria G ^b,c   Martin, Thomas E ^b  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MONTANA   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Allometry; Development; Epigenetic; Maternal effect; Nest predation; Yolk steroids

Indexed keywords

ANDROSTANOLONE; ANDROSTENEDIONE; TESTOSTERONE;

ANDROGEN; CLUTCH SIZE; EMBRYO; MORTALITY; PASSERINE; PREDATION; STEROID;

ANIMAL; ANIMAL EMBRYO; ARTICLE; BODY SIZE; CHEMISTRY; CLUTCH SIZE; EGG YOLK; EMBRYO DEVELOPMENT; FEMALE; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; PREDATION; PRENATAL DEVELOPMENT; SONGBIRD; ZYGOTE;

ANDROSTENEDIONE; ANIMALS; BODY SIZE; CLUTCH SIZE; DIHYDROTESTOSTERONE; EGG YOLK; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; PREDATORY BEHAVIOR; SELECTION (GENETICS); SONGBIRDS; TESTOSTERONE; ZYGOTE;

AVES; PASSERIFORMES;

EID: 34547678023     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/519397     Document Type: Article

References (62)

1. Arnold, A. P. 2002. Concepts of genetic and hormonal induction of vertebrate sexual differentiation in the twentieth century, with special reference to the brain. Pages 105-135 in D. Pfaff, A. Arnold, A. Etgen, S. Fahrbach, and R. Rubin, eds. Hormones, brain, and behavior. Vol. 4. Academic Press, New York.
2. Badyaev, A. V., H. Schwabl, R. L. Young, R. A. Duckworth, K. Navara, and A. F. Parlow. 2005. Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proceedings of the Royal Society B: Biological Sciences 272:2165-2172.
3. Bateson, P., D. Barker, T. Clutton-Brock, D. Deb, B. D'Udine, R. A. Foley, P. Gluckman, et al. 2004. Developmental plasticity and human health. Nature 430:419-421.
4. Bosque, C., and M. T. Bosque. 1995. Nest predation as a selective factor in the evolution of developmental rates in altricial birds. American Naturalist 145:234-260.
5. Briskie, J. V., and S. G. Sealy. 1990. Evolution of short incubation periods in the parasitic cowbirds, Molothrus spp. Auk 107:789-794.
6. Case, T. J. 1978. On the evolution and adaptive significance of postnatal growth rates in terrestrial vertebrates. Quarterly Reviews in Biology 53:243-282.
7. Chen, F., K. Knecht, C. Leu, S. J. Rutledge, A. Scafonas, C. Gambone, R. Vogel, et al. 2004. Partial agonist/antagonist properties of androstenedione and 4-androsten-3β,17β-diol. Journal of Steroid Biochemistry and Molecular Biology 91:247-257.
8. Eising, C. M., C. Eikenaar, H. Schwabl, and T. G. G. Groothuis. 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proceedings of the Royal Society B: Biological Sciences 268:839-846.
9. Eising, C. M., W. Müller, and T. G. G. Groothuis. 2006. Avian mothers create different phenotypes by hormone deposition in their eggs. Biology Letters 2:20-22.
10. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
11. Fleming, T. P., W. Y. Kwong, R. Porter, E. Ursell, I. Fesenko, A. Wilkins, D. J. Miller, A. J. Watson, and J. J. Eckert. 2004. The embryo and its future. Biology of Reproduction 71:1046-1054.
12. Gil, D., J. Graves, N. Hazon, and A. Wells. 1999. Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126-128.
13. Gil, D., C. Biard, A. Lacroix, C. Spottiswoode, N. Saino, M. Puerta, and A. P. Møller. 2007. Evolution of yolk androgens in birds: development, coloniality, and sexual dichromatism. American Naturalist 169:802-819.
14. Gilbert, S. F. 2001. Ecological developmental biology: developmental biology meets the real world. Developmental Biology 233:1-12.
15. Gorman, K. B., and T. D. Williams. 2005. Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds. Biology Letters 1:461-464.
16. Groothuis, T. G., and H. Schwabl. 2002. Determinants of within-and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Functional Ecology 16:281-289.
17. Groothuis, T. G. G., W. Müller, N. von Engelhardt, C. Carere, and C. Eising. 2005. Maternal hormones as a tool to adjust offspring phenotype in avian species. Neuroscience and Biobehavioral Reviews 29:329-352.
18. Gwinner, H., and H. Schwabl. 2005. Evidence for sexy sons in European starlings (Sturnus vulgaris). Behavioral Ecology and Sociobiology 58:375-382.
19. Harding, C. 1998. Androgens, effects in birds. Pages 188-196 in E. Knobil and J. D. Neill, eds. Encyclopedia of reproduction. Vol. 1. Academic Press, San Diego, CA.
20. Hauber, M. E., and K. M. Pilz. 2003. Yolk testosterone levels are not consistently higher in the egg of obligate brood parasites than their hosts. American Midland Naturalist 149:354-362.
21. Hayward, L. S., and J. C. Wingfield. 2004. Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. General and Comparative Endocrinology 135:365-371.
22. Hensler, G. L., and J. D. Nichols. 1981. The Mayfield method of estimating nesting success: a model, estimators and simulation results. Wilson Bulletin 93:42-53.
23. Hiipakka, R. A., and S. Liao. 1998. Dihydrotestosterone. Pages 872-879 in E. Knobil and J. D. Neill, eds. Encyclopedia of reproduction. Vol. 1. Academic Press, San Diego, CA.
24. Holterhus, P. M., S. Piefke, and O. Hiort. 2002. Anabolic steroids, testosterone-precursors and virilizing androgens induce distinct activation profiles of androgen responsive promoter constructs. Journal of Steroid Biochemistry and Molecular Biology 82:269-275.
25. Hoyt, D. F. 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73-77.
26. Jasuja, R., P. Ramaraj, R. Phong Mac, A. B. Singh, T. W. Storer, J. Artaza, A. Miller, et al. 2005. Δ-4-androstene-3,17-dione binds androgen receptor, promotes myogenesis in vitro, and increases serum testosterone levels, fat-free mass, and muscle strength in hypogonadal males. Journal of Clinical Endocrinology and Metabolism 90:855-863.
27. Johnson, A. L. 2000. Female reproduction. Pages 569-591 in G. C. Whittow, ed. Sturkie's avian physiology. 5th ed. Academic Press, San Diego, CA.
28. Ketterson, E. D., V. Nolan Jr., and M. Sandell. 2005. Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both? American Naturalist 166(suppl.):S85-S98.
29. Lipar, J. L., E. D. Ketterson, and V. Nolan Jr. 1999. Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk 116:231-235.
30. Martin, T. E. 1992. Breeding productivity considerations: what are the appropriate habitat features for management? Pages 455-473 in J. M. Hagan and D. W. Johnston, eds. Ecology and conservation of Neotropical migrants. Smithsonian Institution, Washington, DC.
31. _. 1995. Avian life-history evolution in relation to nest sites, nest predation, and food. Ecological Monographs 65:101-127.
32. _. 2002. A new view of avian life history tested on an incubation paradox. Proceedings of the Royal Society B: Biological Sciences 269:309-316.
33. Martin, T. E., J. Scott, and C. Menge. 2000. Nest predation increases with parental activity: separating nest site and parental activity effects. Proceedings of the Royal Society B: Biological Sciences 267:2287-2294.
34. Martin, T. E., R. D. Bassar, S. K. Bassar, J. J. Fontaine, P. Lloyd, H. Mathewson, A. Niklison, and A. Chalfoun. 2006. Life history and ecological correlates of geographic variation in egg and clutch mass among passerine species. Evolution 60:390-398.
35. Mayfield, H. 1975. Suggestions for calculating nest success. Wilson Bulletin 87:456-466.
36. McCormick, C. M., B. F. Furey, M. Child, M. J. Sawyer, and S. M. Donohue. 1998. Neonatal sex hormones have "organizational" effects on the hypothalamic-pituitary-adrenal axis of male rats. Developmental Brain Research 105:295-307.
37. Metcalfe, N. B., and P. Monaghan. 2003. Growth versus lifespan: perspectives from evolutionary ecology. Experimental Gerontology 38:935-940.
38. Mousseau, T. A., and C. W. Fox. 1998. Maternal effects as adaptations. Oxford University Press, New York.
39. Müller, W., T. G. G. Groothuis, A. Kasprzik, C. Dijkstra, R. V. Alatalo, and H. Siitari. 2005. Prenatal androgen exposure modulates cellular and humoral immune function of black-headed gull chicks. Proceedings of the Royal Society B: Biological Sciences 272:1971-1977.
40. Navara, K. J., Hill, G. E., and M. T. Mendonça. 2005. Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiological and Biochemical Zoology 78:570-578.
41. Payne, A. H., and D. B. Hales. 2004. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Reviews 25:947-970.
42. Pilz, K. M., H. G. Smith, M. I. Sandell, and H. Schwabl. 2003. Interfemale variation in egg yolk androgen allocation in the European starling: do high-quality females invest more? Animal Behaviour 65:841-850.
43. Poopatanapong, A. 2002. Relationship between male badge size and female reproductive investment and mate choice in house sparrow. MS thesis. Washington State University, Pullman.
44. Purvis, A., and A. Rambaut. 1995. Comparative analysis by independent contrast (CAIC): an Apple-Macintosh application for analyzing comparative data. Computer and Applied Biological Sciences 11:247-251.
45. Remeš, V., and T. E. Martin. 2002. Environmental influences on the evolution of growth and developmental rates in passerines. Evolution 56:2505-2518.
46. Romanoff, A. L. 1944. Avian spare yolk and its assimilation. Auk 61:235-241.
47. Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing birds. Proceedings of the National Academy of Sciences of the USA 90:11439-11441.
48. _. 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comparative and Biochemical Physiology A 114:271-276.
49. _. 1997. Maternal steroid hormones in the egg. Pages 3-13 in R. Etches and S. Harvey, eds. Perspectives in avian endocrinology. Journal of Endocrinology, Bristol, UK.
50. _. 1999. Developmental changes and among-sibling variation of corticosterone levels in an altricial avian species. General and Comparative Endocrinology 116:403-408.
51. Sibley, C. G., and J. E. Ahlquist. 1990. Phylogeny and classification of birds. Yale University Press, New Haven, CT.
52. Sockman, K. W., and H. Schwabl. 2000. Yolk androgens reduce offspring survival. Proceedings of the Royal Society B: Biological Sciences 267:1451-1456.
53. _. 2001. Plasma corticosterone in nestling American kestrels: effects of age, handling stress, yolk androgens, and body condition. General and Comparative Endocrinology 122:205-212.
54. Sonneveld, E., H. J. Jansen, J. A. C. Riteco, A. Brouwer, and B. van der Burg. 2005. Development of androgen- and estrogen-response bioassays, members of a panel of human cell line-based highly selective steroid-responsive bioassays. Toxicological Sciences 83:136-148.
55. Sonneveld, E., J. A. C. Riteco, H. J. Jansen, B. Pieterse, A. Brouwer, W. G. Schoonen, and B. van der Burg. 2006. Comparison of in vitro and in vivo screening models for androgenic and estrogenic activities. Toxicological Sciences 89:173-187.
56. Staub, N. L., and M. DeBeer. 1997, The role of androgens in female vertebrates. General and Comparative Endocrinology 108:1-24.
57. Strasser, R., and H. Schwabl. 2004. Yolk testosterone modifies the expression of sexually selected traits in sons. Behavioral Ecology and Sociobiology 56:491-497.
58. Tschirren, B., H. Richner, and H. Schwabl. 2004. Ectoparasite-modulated deposition of maternal androgens in great tit eggs. Proceedings of the Royal Society 3: Biological Sciences. 271:1371-1375.
59. Tschirren, B., V. Saladin, P. S. Fitze, H. Schwabl, and H. Richner. 2005. Maternal yolk testosterone does not modulate parasite susceptibility or immune function in great tit nestlings (Parus major). Journal of Animal Ecology 74:675-682.
60. von Engelhardt, N., C. Carere, C. Dijkstra, and T. G. G. Groothuis. 2006. Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches. Proceedings of the Royal Society B: Biological Sciences 273:65-70.
61. Welberg, L. A. M., and J. R. Seckl. 2001. Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology 13:113-128.
62. Whittingham, L. A., and H. Schwabl. 2002. Maternal testosterone in tree swallow egg varies with female aggression. Animal Behaviour 63:63-67.