Evolution of sex-biased maternal effects in birds: I. Sex-specific resource allocation among simultaneously growing oocytes

Journal of Evolutionary Biology

Volumn 17, Issue 6, 2004, Pages 1355-1366

  Young, R L ^a   Badyaev, A V ^a,b  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Egg laying order; Follicles; Life history trade off; Maternal effects; Oocyte growth; Ovulation; Rapid yolk deposition; Yolk size

Indexed keywords

EVOLUTION; MATERNAL EFFECT; PASSERINE; RESOURCE ALLOCATION; TRADE-OFF;

ANIMAL; ARTICLE; COMPARATIVE STUDY; EVOLUTION; FEMALE; FINCH; GENDER AND SEX; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; MALE; MORPHOMETRICS; OOCYTE; OVULATION; PHYSIOLOGY; REPRODUCTION; SEX DIFFERENCE;

ANIMALS; BODY WEIGHTS AND MEASURES; EVOLUTION; FEMALE; FINCHES; MALE; OOCYTES; OVULATION; REPRODUCTION; SELECTION (GENETICS); SEX DETERMINATION (GENETICS); SEX FACTORS;

AVES; CARPODACUS; CARPODACUS MEXICANUS; FRINGILLIDAE; PASSERIFORMES; VERTEBRATA;

EID: 8144229844     PISSN: 1010061X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2004.00762.x     Document Type: Article

References (106)

1. Adkins-Regan, E., Ottinger, M.A. & Park, J. 1995. Maternal transfer of estradiol to egg yolk alters sexual differentiation of avian offspring. J. Exp. Zool. 271: 466-470.
2. Anderson, D.J., Reeve, J. & Bird, D.M. 1997. Sexually dimorphic eggs, nestling growth and sibling competition in American Kestrels Falco sparverius. Funct. Ecol. 11: 331-335.
3. Anderson, M., Wallander, J., Oring, L., Akst, E., Reed, J.M. & Fleischer, R.C. 2003. Adaptive seasonal trend in brood sex ratio: test in two sister species with contrasting breeding systems. J. Evol. Biol. 16: 510-515.
4. Ankney, C.D. 1982. Sex ratio varies with egg sequence in lesser snow geese. Auk 99: 662-666.
5. Arnold, K.E., Orr, K.J. & Griffiths, R. 2003. Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs. Mol. Ecol. 12: 3451-3458.
6. Astheimer, L.B. & Grau, C.R. 1990. A comparison of yolk growth rates in seabird eggs. Mol. Ecol. 132: 380-394.
7. Astheimer, L.B., Prince, P.A. & Grau, C.R. 1985. Egg formation and the pre-laying period of Black-browed and Grey-headed Albatrosses Diomedea melanophris and D. chrysostoma at Bird Island, South Georgia. Mol. Ecol. 127: 523-529.
8. Badyaev, A.V. & Martin, T.E. 2000. Sexual dimorphism in relation to current selection in the house finch. Evolution 54: 987-997.
9. Badyaev, A.V., Hill, G.E. & Whittingham, L.A. 2001a. The evolution of sexual size dimorphism in the house finch: IV. Population divergence in ontogeny of dimorphism. Evolution 55: 2534-2549.
10. Badyaev, A.V., Whittingham, L.A. & Hill, G.E. 2001b. The evolution of sexual size dimorphism in the house finch: III. Developmental basis. Evolution 55: 176-189.
11. Badyaev, A.V., Hill, G.E., Beck, M.L., Dervan, A.A., Duckworth, R.A., McGraw, K.J., Nolan, P.M. & Whittingham, L.A. 2002. Sex-biased hatching order and adaptive population divergence in a passerine bird. Science 295: 316-318.
12. Badyaev, A.V., Beck, M.L., Hill, G.E. & Whittingham, L.A. 2003a. The evolution of sexual size dimorphism in the house finch: V. Maternal effects. Evolution 57: 384-396.
13. Badyaev, A.V., Hill, G.E. & Beck, M.L. 2003b. Interaction between maternal effects: onset of incubation is related to offspring sex in a passerine bird. Oecologia 135: 386-390.
14. Bahr, J.M., Wang, S.-C., Huang, M.Y. & Calvo, F.O. 1983. Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol. Reprod. 29: 326-334.
15. Barber, D.L., Sanders, E.J., Aebersold, R. & Schneider, W.J. 1991. The receptor for yolk lipoprotein deposition in the chicken oocyte. J. Biol. Chem. 266: 18761-18770.
16. Birrenkott, G.P., Shoop, M.A., Cooper, K. & Wiggens, M. 1988. Ovarian follicular growth and maturation in the Domestic Pigeon and Guinea Fowl (Numida meleagris). Poult. Sci. 67: 1783-1786.
17. Bissonnette, T.H. & Zujko, A.J. 1936. Normal progressive changes in the ovary of the Starling (Sturnus vulgaris) from December to April. Auk 53: 31-50.
18. Blanco, G., Dávila, J.A., López Septiem, J.A., Rodríguez, R. & Martínez, F. 2002. Sex-biased initial eggs favour sons in the slightly size-dimorphic Scops owl (Otus scops). Biol. J. Linnean Soc. 76: 1-7.
19. Blanco, G., Martinez-Padilla, J., Davila, J.A., Serrano, D. & Vinuela, J. 2003. First evidence of sex differences in the duration of avian embryonic period: consequences for sibling competition in sexually dimorphic birds. Behav. Ecol. 14: 702-706.
20. Bortolotti, G.R. 1986. Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am. Nat. 127: 495-507.
21. Bortolotti, G.R., Negro, J.J., Surai, P.F. & Prieto, P. 2003. Carotenoids in eggs and plasma of red-legged partridges: effects of diet and reproductive output. Physiol. Biochem. Zool. 76: 367-374.
22. Bowden, R.M., Ewert, M.A. & Nelson, C.E. 2000. Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc. R. Soc. Lond. B 267: 1745-1749.
23. Bowden, R.M., Ewert, M.A., Lipar, J.L. & Nelson, C.E. 2001. Concentrations of steroid hormones in layers and biopsies of chelonian egg yolks. Gen. Comp. Endocrinol. 121: 95-103.
24. Bray, D.F. 1965. Embryonic weight as a selection criterion in alteration of growth curves of domestic birds - data from the domestic turkey. Can. J. Gen. Cytol. 7: 1-11.
25. Burke, W.H. 1989. Sex differences in body weight of chicken embryos. Poult. Sci. 68: 805-810.
26. Burke, W.H. 1992. Sex differences in incubation length and hatching weights of broiler chicks. Poult. Sci. 71: 1933-1938.
27. Burley, R.W. & Vadehra, D.V. 1989. The Avian Egg: Chemistry and Biology. John Wiley & Sons, New York.
28. Challenger, W.O., Williams, T.D., Christians, J.K. & Vezina, F. 2001. Follicular development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris). Physiol. Biochem. Zool. 74: 356-365.
29. Conley, A.J. 1997. Yolk steroids decline during sexual differentiation in the alligator. Gen. Comp. Endocrinol 107: 191-200.
30. Cordero, P.J., Griffith, S.C., Aparicio, J.M. & Parkin, D.T. 2000. Sexual dimorphism in house sparrow eggs. Behav. Ecol. Sociobiol. 48: 353-357.
31. Cordero, P.J., Vinuela, J., Aparicio, J.M. & Veiga, J.P. 2001. Seasonal variation in sex ratio and sexual egg dimorphism favouring daughters in first clutches of the spotless starling. J. Evol. Biol. 14: 829-834.
32. Crisostomo, S., Guemene, D., Garreau-Mills, M., Morvan, C. & Zadworny, D. 1998. Prevention of incubation behavior expression in turkey hens by active immunization against prolactin. Theriogenology 50: 675-690.
33. Dijkstra, C., Daan, S. & Buker, J.B. 1990. Adaptive seasonal variation in the sex ratio of kestrel broods. Funct. Ecol. 4: 143-147.
34. Doi, O., Takai, T., Nakamura, T. & Tanabe, Y. 1980. Changes in pituitary and plasma LH, plasma and follicular progesterone and estradiol and plasma testosterone and estrone concentrations during the ovulatory cycle of the quail (Coturnix coturnix japonica). Gen. Comp. Endocrinol. 41: 156-163.
35. Dzus, E.H., Bortolotti, G.R. & Gerrard, J.M. 1996. Does sex-biased hatching order in bald eagles vary with food resources? Ecoscience 3: 252-258.
36. Eising, C.M., Eikenaar, C., Schwabl, H. & Groothuis, G.G. 2001. Maternal antrogens in black-headed gull (Larus ridibunus) eggs: consequences for chick development. Proc. R. Soc. Biol. Sci. B 268: 839-846.
37. Ellegren, H., Gustafsson, L. & Sheldon, B.C. 1996. Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc. Natl. Acad. Sci. USA 93: 11723-11728.
38. Etches, R.J. & Duke, C.E. 1984. Progesterone, androstenedione and estradiol content of theca and granulosa tissues of the four largest ovarian follicles during the ovulatory cycle of the hen (Gallus domesticus). J. Endocrinol. 103: 71-76.
39. Grau, C.R. 1976. Ring structure of avian egg yolk. Poult. Sci. 55: 1418-1422.
40. Grau, C.R. 1996. Nutritional needs for egg formation in the Shag Phalacrocorax aristotelis. Poult. Sci. 138: 756-764.
41. Griffiths, R., Daan, S. & Dijkstra, C 1996. Sex identification in birds using two CHD genes. Proc. R. Soc. Biol. Sci. B 263: 1251-1256.
42. Griffiths, R., Double, M., Orr, K. & Dawson, R. 1998. A DNA test to sex most birds. Mol. Ecol. 7: 1071-1076.
43. Heath, D.D., Heath, J.W., Bryden, C.A., Johnson, R.M. & Fox, C.W. 2003. Rapid evolution of egg size in captive salmon. Science 299: 1738-1740.
44. Hillström, L. 1999. Variation in egg mass in the pied flycather, Ficedula hypoleuca: an experimental test of the brood survival and brood reduction hypothesis. Evol. Ecol. Res. 1: 753-768.
45. Johnson, A.L. 1996. The avian ovarian hierarchy: a balance between follicle differentiation and atresia. Poult. Avian Biol. Rev. 7: 99-110.
46. Koutsos, E.A., Clifford, A.J., Calvert, C.C. & Klasing, K.C. 2003. Maternal carotenoid status modifies the incorporation of dietary carotenoids into immune tissues of growing chickens (Callus gallus domesticus). J. Nutr. 133: 1132-1138.
47. Krackow, S. 1995. The developmental asynchrony hypothesis for sex ratios manipulations. J. Theor. Biol. 176: 273-280.
48. Krebs, E.A., Green, D.J., Double, M.C. & Griffiths, R. 2002. Laying date and laying sequence influence the sex ratio of cromson rosella broods. Behav. Ecol. Sociobiol. 51: 447-454.
49. Leimar, O. 1996. Life-history analysis of the Trivers and Willard sex-ratio problem. Behav. Ecol. 7: 316-325.
50. Lipar, J.L. & Ketterson, E.D. 2000. Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc. R. Soc. Biol. Sci. B 267: 2005-2010.
51. Lovern, M. & Wade, J. 2003. Yolk testosterone varies with sex in eggs of the lizard, Anolis carolinensis. J. Exp. Biol. 295A: 206-210.
52. Magrath, R.D. 1992. Seasonal changes in egg-mass within and among clutches of birds: general explanations and a field study of the Blackbird Turdus merula. J. Exp. Biol. 134: 171-179.
53. Magrath, M.J.L., Brouwer, L. & Komdeur, J. 2003. Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic songlark, Cinclorhamphus cruralis. Behav. Ecol. Sociobiol. 54: 240-248.
54. Maney, D.L., Hahn, T.P., Schoech, S.J., Sharp, P.J., Morton, M.L. & Wingfield, J.C. 1999. Effects of ambient temperature on photo-induced prolactin secretion in three subspecies of White-crowned sparrow, Zonotrichia leucophrys. Gen. Comp. Endocrinol. 113: 445-456.
55. Mead, P.S. & Morton, M.L. 1985. Hatching asynchrony in the mountain white-crowned sparrow (Zonotrichia leucophyris oriantha): a selected or incidental trait? Auk 102: 781-792.
56. Mead, P.S., Morton, M.L. & Fish, B.E. 1987. Sexual dimorphism in egg size and implications regarding facultative manipulation of sex in mountain white-crowned sparrows. Condor 89: 798-803.
57. Meathrel, C.E. 1991. Variation in eggs and the period of rapid yolk deposition of the silver gull Larus novaehollandiae during a protracted laying season. J. Zool. 223: 501-508.
58. Mittwoch, U. 1993. Blastocysts prepare for the race to be male. Hum. Reprod. 8: 1550-1555.
59. Monaghan, P., Nager, R.G. & Houston, D.C. 1998. The price of eggs: increased investment in egg production reduces the offspring rearing capacity of parents. Proc. R. Soc. Biol. Sci. B 265: 1731-1735.
60. Müller, W., Eising, C.M., Dijkstra, C. & Groothuis, T.G.G. 2002. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Callus gallus domesticus). Proc. R. Soc. Lond. B 269: 2249-2255.
61. Müller, W., Dijkstra, C. & Groothuis, T.G.G. 2003. Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ribidundus) depend on the hatching order. Behav. Ecol. Sociobiol. 55: 80-86.
62. Nager, R.G., Managhan, P., Griffiths, R., Houston, D.C. & Dawson, R. 1999. Experimental demonstration that offspring sex ratio varies with maternal condition. Proc. Natl. Acad. Sci. USA 96: 570-573.
63. Nager, R.G., Monaghan, P. & Houston, D.C. 2001. The cost of egg production: Increased egg production reduces future fitness in gulls. J. Avian Biol. 32: 159-166.
64. Olsen, M.W. 1942. Maturation, fertilization, and early cleavage in the hen's egg. J. Morphol. 70: 513-528.
65. Olsen, M.W. & Fraps, R.M. 1944. Maturation, fertilization, and early cleavage of the egg of the Domestic Turkey. J. Morphol. 74: 297-309.
66. Parks, J.S. 2001. The ontogeny of growth hormone sensitivity. Horm. Res. 55: 27-31.
67. Parsons, J. 1975. Asynchronous hatching and chick mortality in the Herring Gull Larus argentatus. Horm. Res. 117
68. Petrie, M., Schwabl, H., Brande-Lavridsen, N. & Burke, T. 2001. Sex differences in avian yolk hormone levels. Nature 412: 498.
69. Porter, T.E., Hargis, B.M., Silsby, J.L. & el Halawani, M.E. 1989. Differential steroid production between theca interna and theca externa cells: a three-cell model for follicular steroidogenesis in avian species. Endocrinology 125: 109-116.
70. Ray, P.F., Conaghan, J., Winston, R.M.L. & Handyside, A.H. 1995. Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization. J. Reprod. Fertil. 104: 165-171.
71. Redshaw, M.R. & Follet, B.K. 1976. Physiology of egg yolk production by the fowl: the measurement of circulating levels of vitellogenin employing a specific radioimmunoassay. Comp. Biochem. Physiol. 55A: 399-405.
72. Robinson, F.E. & Etches, R.J. 1986. Ovarian steroidogenesis during follicular maturation in the domestic fowl (Gallus domesticus). Biol. Reprod. 35: 1096-1105.
73. Roosenburg, W.M. 1996. Maternal condition and nest site choice: an alternative for the maintenance of environmental sex determination? Am. Zool. 36: 157-168.
74. Royle, N.J. & Hamer, K.C. 1998. Hatching asynchrony and sibling size hierarchies in gulls: effects on parental investment decisions, brood reduction and reproductive success. J. Avian Biol. 29: 266-272.
75. Royle, N., Surai, P.F., McCartney, R.J. & Speake, B.K. 1999. Parental investment and egg yolk lipid composition in gulls. Funct. Ecol. 13: 298-306.
76. Rutkowska, J. & Cichon, M. 2002. Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim. Behav. 64: 817-822.
77. Ryder, J.P. 1983. Sex ratio and egg sequence in Ring-billed gulls. Auk 100: 726-730.
78. Saino, N., Romano, M., Ferrari, R.P., Martinelli, R. & Moller, A.P. 2003. Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex. J. Evol. Biol. 516-522
79. Sasvári, L., Hegyi, Z. & Péczely, P. 1999. Brood reduction in white storks mediated through asymmetries in plasma testosterone concentrations in chicks. Ethology 105: 569-582.
80. Schwabl, H. 1993. Yolk is a source of maternal testosterone for developing birds. Proc. Natl. Acad. Sci. USA 90: 11446-11450.
81. Schwabl, H. 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comp. Biochem. Physiol. 114: 271-276.
82. Schwabl, H., Mock, D.W. & Gieg, J.A. 1997. A hormonal mechanism for parental favoritism. Nature 386: 231.
83. Shahabi, N.A., Norton, H.W. & Nalbandov, A.V. 1975. Steroid levels in follicles and the plasma of hens during the ovulatory cycle. Endocrinology 96: 962-968.
84. Sockman, K.W. & Schwabl, H. 1999. Daily estradiol and progesterone levels relative to laying and onset of incubation in canaries. Gen. Comp. Endocrinol. 114: 257-268.
85. Sockman, K.W., Schwabl, H. & Sharp, P.J. 2000. The role of prolactin in the regulation of clutch size and onset of incubation behavior in the American Kestrel. Horm. Behav. 38: 168-178.
86. Sockman, K.W., Schwabl, H. & Sharp, P.J. 2001. Regulation of yolk-androgen concentrations by plasma prolactin in the American Kestrel. Horm. Behav. 40: 462-471.
87. Stamps, J.A. 1990. When should avian parents differentially provision sons and daughters? Am. Nat. 135: 671-685.
88. Stearns, S.C. 1976. Life-history tactics: a review of the ideas. Q. Rev. Biol. 51: 3-47.
89. Sturkie, P.D. 1986. Avian Physiology. Springer, Berlin.
90. Surai, P.F., Ionov, I.A., Kuklenko, T.V., Kostjuk, I.A., MacPherson, A., Speake, B.K., Noble, R.C. & Sparks, N.H.C. 1998. Effect of supplementing the hen's diet with vitamin A on the accumulation of vitamins A and E, ascorbic acid and carotenoids in the egg yolk and in the embryonic liver. Br. Poult. Sci. 39: 257-263.
91. Trivers, R.L. & Willard, D.E. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179: 90-91.
92. Uller, T. 2003. Viviparity as a constraint on sex-ratio evolution. Evolution 57: 927-931.
93. Velando, A. 2002. Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby. Behav. Ecol. 13: 443-449.
94. Velando, A., Graves, J. & Ortega-Ruano, J. 2002. Sex ratio in relation to timing of breeding, and laying sequence in a dimorphic seabird. Behav. Ecol. 144: 9-16.
95. Vezina, F. & Williams, T.D. 2002. Metabolic costs of egg production in the European starling (Sturnus vulgaris). 377-385.
96. Visser, M.E. & Lessells, C.M. 2001. The costs of egg production and incubation in great tits (Parsus major). Proc. R. Soc. Lond. B 268: 1271-1277.
97. Warren, D.C. & Scott, H.M. 1935. The time factor in egg formation. Poult. Sci. 14: 195-207.
98. West, S.A. & Sheldon, B.C. 2002. Constraints in the evolution of sex ratio adjustment. Science 295: 1685-1688.
99. Whittingham, L.A. & Schwabl, H. 2002. Maternal testosterone in tree swallow eggs varies with female aggression. Anim. Behav. 63: 63-67.
100. Williams, G.C. 1966. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press, Princeton.
101. Williams, T.D. 2001. Experimental manipulation of female reproduction reveals an intraspecific egg size-clutch size trade-off. Proc. R. Soc. Lond. B 268: 423-428.
102. Williams, T.D. & Cooch, E.G. 1996. Egg size, temperature and laying sequence: why do snow geese lay big eggs when it's cold? Funct. Ecol. 10: 112-118.
103. Yoshimura, Y., Okamotoa, T. & Tamura, T. 1993a. Electron microscope observations on LH-induced oocyte maturation in Japanese Quail (Coturnix coturnix japonica). J. Reprod. Fertil. 98: 401-407.
104. Yoshimura, Y., Okamotoa, T. & Tamura, T. 1993b. Ultrastructural changes of oocyte and follicular wall during oocyte maturation in the Japanese Quail (Coturnix coturnix japonica). J. Reprod. Fertil. 97: 189-196.
105. Zadworny, D., Shimada, K., Ishida, H. & Sato, K. 1986. Gonadotropin-stimulated estradiol production in small ovarian follicles of the hen in suppressed by physiological concentrations of prolactin in vitro. Gen. Comp. Endocrinol. 74: 468-473.
106. Zann, R.A. 1996. The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford University Press, Oxford.