Skip main navigationJournal menuClose Drawer MenuOpen Drawer Menu
Skip main navigationJournal menuClose Drawer MenuOpen Drawer Menu
Biology Letters
Restricted access

High progesterone during avian meiosis biases sex ratios toward females

Published:13 May 2005https://doi.org/10.1098/rsbl.2004.0283

    Abstract

    Evidence of altered primary sex ratios in birds shows that mothers can manipulate the sex of their offspring before oviposition. In birds, females are the heterogametic sex (ZW) and males are homogametic (ZZ). Sex is determined in the first meiotic division, when one sex chromosome is retained in the oocyte and the other segregates to the polar body. Altered primary sex ratios suggest that birds may be capable of biasing the segregation of sex chromosomes during meiosis I. During the time of meiosis I, follicular steroid production is limited primarily to progesterone (P4). We experimentally manipulated the levels of P4 in female domestic chickens during the approximate time of meiosis I. We advanced the ovulation of the first egg of a sequence (or clutch) with a subcutaneous injection of P4. We found a significant effect of P4 dose on the sex of the resulting egg. The high progesterone group produced 25% males whereas the low progesterone group produced 61% males and the control group produced 63% males in the first ovulation of the sequence. We propose that variation in maternal progesterone during the critical time for genetic sex determination is the mechanism for primary sex ratio manipulation in birds.

    References

    • Ahmad G& Zamenof S. 1979Effect of progesterone on brain and body growth of chick-embryos. Growth 43, 58–61. PubMed, Google Scholar
    • Bluhm C.K, Phillips R.E& Burke W.HSerum levels of luteinizing hormone, prolactin, estradiol, and progesterone in laying and nonlaying Mallards, Anas platyrhynchos. Biol. Reprod 281983a295–305. Crossref, PubMed, ISI, Google Scholar
    • Bluhm C.K, Phillips R.E& Burke W.HSerum levels of luteinizing hormone (LH), prolactin, estradiol, and progesterone in laying and nonlaying Canvasback ducks (Aythya valisineria). J. Zool. (Lond.) 2041983b185–200. Crossref, Google Scholar
    • Boada L.D, Zumbado M, del Rio I, Blanco A, Torres S, Monterde J.G, Afonso J.L, Cabrera J.J& Diaz-Chico B.N. 2002Steroid hormone progesterone induces cell proliferation and abnormal mitotic processes in rat liver. Arch. Toxicol 75, 707–716. Crossref, PubMed, ISI, Google Scholar
    • Cameron E.Z& Linklater W.L. 2002Sex bias in studies of sex bias: the value of daughters to mothers in poor condition. Anim. Behav 63, F5–F8. Crossref, Google Scholar
    • Cockrem J.F& Sneddon P.J. 1994Annual cycle of sex steroids in the yellow-eyed penguin (Megadyptes antipodes) on South Island, New Zealand. Gen. Comp. Endocrinol 94, 113–121. Crossref, PubMed, ISI, Google Scholar
    • Etches R& Duke C. 1984Progesterone, androstenedione and estradiol content of theca and granulosa tissues of the four largest ovarian follicles during the ovulatory cycle of the hen. J. Endocrinol 103, 71–76. Crossref, PubMed, ISI, Google Scholar
    • Griffiths R, Double M, Orr K& Dawson R. 1998A DNA test to sex most birds. Mol. Ecol 7, 1071–1075. Crossref, PubMed, ISI, Google Scholar
    • Heath J.A, Frederick P.C, Edwards T.M& Guillette L.J. 2003Reproductive physiology of free-living white ibises (Eudocimus albus) in the Florida everglades. Gen. Comp. Endocrinol 133, 118–131. Crossref, PubMed, ISI, Google Scholar
    • Johnson A.L& van Tienhoven A. 1980Plasma concentrations of six steroids and LH during the ovulatory cycle of the hen, Gallus domesticus. Biol. Reprod 23, 386–393. Crossref, PubMed, ISI, Google Scholar
    • Komdeur J, Daan S, Tinbergen J& Mateman C. 1997Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature 385, 522–525. Crossref, ISI, Google Scholar
    • Lea R.W, Vowles D.M& Dick H.R. 1986Factors affecting prolactin secretion during the breeding cycle of the ring dove (Streptopelia risoria) and its possible role in incubation. J. Endocrinol 110, 447–458. Crossref, PubMed, ISI, Google Scholar
    • LeMaire-Adkins R& Hunt P.A. 2000Nonrandom segregation of the mouse univalent X chromosome: evidence of spindle-mediated meiotic drive. Genetics 156, 775–783. Crossref, PubMed, ISI, Google Scholar
    • Logan C.A& Wingfield J.C. 1995Hormonal correlates of breeding status, nest construction, and parental care in multiple-brooded northern mockingbirds, Mimus polyglottos. Horm. Behav 29, 12–30. Crossref, PubMed, ISI, Google Scholar
    • Mauget R, Jouventin P, Lacroix A& Ishii S. 1994Plasma LH and steroid hormones in king penguins (Aptenodytes patagonicus) during the onset of the breeding cycle. Gen. Comp. Endocrinol 93, 36–43. Crossref, PubMed, ISI, Google Scholar
    • Müller W, Eising C.M, Dijkstra C& Groothuis T.G.G. 2002Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc. R. Soc. B 269, 2249–2255.doi:10.1098/rspb.2002.2159. Link, ISI, Google Scholar
    • Olsen M& Fraps R.M. 1950Maturation changes in the hen's ovum. J. Exp. Zool 144, 475–487. Crossref, Google Scholar
    • Pardo-Manuel de Villena F& Sapienza C. 2001Nonrandom segregation during meiosis: the unfairness of females. Mamm. Genome 12, 331–339. Crossref, PubMed, ISI, Google Scholar
    • Parker T.H. 2002Maternal condition, reproductive investment, and offspring sex ratio in captive red junglefowl (Gallus gallus). Auk 119, 840–845. Crossref, ISI, Google Scholar
    • Petrie M, Schwabl H, Brande-Lavridsen N& Burke T. 2001Sex differences in avian yolk hormone levels. Nature 412, 489. Crossref, PubMed, ISI, Google Scholar
    • Pike T.W& Petrie M. 2003Potential mechanisms of avian sex manipulation. Biol. Rev 78, 553–574. Crossref, PubMed, ISI, Google Scholar
    • Rehder N.B, Bird D.M& Lague P.C. 1986Variations in plasma corticosterone, estrone, estradiol-17β, and progesterone concentrations with forced renesting, molt and body weight of captive female American kestrels. Gen. Comp. Endocrinol 62, 386–393. Crossref, PubMed, ISI, Google Scholar
    • Renden J.A& Benoff F.H. 1980Effects of progesterone on developing chick embryos. Poult. Sci 59, 2559–2563. Crossref, PubMed, ISI, Google Scholar
    • Seiler H.W, Gahr M, Goldsmith A.R& Güttinger H.R. 1992Prolactin and gonadal steroids during the reproductive cycle of the Bengalese finch (Lonchura striata var domestica, Estrildidae), a nonseasonal breeder with biparental care. Gen. Comp. Endocrinol 88, 83–90. Crossref, PubMed, ISI, Google Scholar
    • Sharp P.J, Lea R.W, Chadwick A& Lake P.E. 1981Concentrations of plasma luteinising hormone, prolactin, progesterone and androgens during the ovulatory cycle of the turkey. Br. Poult. Sci 22, 375–383. Crossref, PubMed, ISI, Google Scholar
    • Trivers R& Willard D. 1973Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–92. Crossref, PubMed, ISI, Google Scholar
    • von Engelhardt N, Dijkstra C, Daan S& Groothuis T.G.G. 2004Effects of 17-beta-estradiol treatment of female zebra finches on offspring sex ratio and survival. Horm. Behav 45, 306–313. Crossref, PubMed, ISI, Google Scholar
    • Wilson, K. & Hardy, I. 2002 Statistical analysis of sex ratios: an introduction. In Sex ratios: concepts and research methods (ed. I. Hardy), pp. 48–92. Cambridge University Press. Google Scholar
    • Wingfield, J. C. & Farner, D. S. 1993 Endocrinology of reproduction in wild species In Avian biology, vol. IX (ed. D. S. Farner, J. R. King & K. C. Parkes), p. 222. London: Academic Press. Google Scholar
    • Yoshimura Y, Koike K& Okamoto T. 2000Immunolocalization of progesterone and estrogen receptors in the sperm storage tubules of laying and diethylstilbestrol-injected immature hens. Poult. Sci 79, 94–98. Crossref, PubMed, ISI, Google Scholar
    Previous Article
    Next Article