The human sex ratio from conception to birth

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 16, 2015, Pages E2102-E2111

  Orzack, Steven Hecht ^a   Stubblefield, J William ^a   Akmaev, Viatcheslav R ^b   Colls, Pere ^c   Munné, Santiago ^c   Scholl, Thomas ^b   Steinsaltz, David ^d   Zuckerman, James E ^e  

^a Fresh Pond Research Institute Cambridge   (United States)

^b Genzyme Genetics ^*  (United States)

^c Reprogenetics LLC   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Demography; Development; Evolution; Genetics; Sex ratio

Indexed keywords

AMNIOCENTESIS; ARTICLE; BIRTH; CHORION VILLUS SAMPLING; CONCEPTION; CONTROLLED STUDY; EMBRYO; FEMALE; FETUS DEATH; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN EMBRYO; INDUCED ABORTION; LIVE BIRTH; MALE; PRIORITY JOURNAL; SEX RATIO; AGE; ANIMAL EMBRYO; FERTILIZATION; INFERTILITY THERAPY; KARYOTYPING; PHYSIOLOGY; PREGNANCY;

ABORTION, INDUCED; AGE FACTORS; CHORIONIC VILLI SAMPLING; EMBRYO, MAMMALIAN; FEMALE; FERTILIZATION; HUMANS; KARYOTYPING; MALE; PARTURITION; PREGNANCY; PREGNANCY TRIMESTER, FIRST; REPRODUCTIVE TECHNIQUES, ASSISTED; SEX RATIO;

EID: 84928243122     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416546112     Document Type: Article

References (122)

1. Graunt J (1662) Natural and Political Observations Made Upon the Bills of Mortality (Martyn, London).
2. Campbell RB (2001) John Graunt, John Arbuthnott, and the human sex ratio. Hum Biol 73(4):605-610.
3. Nichols JB (1907) The numerical proportions of the sexes at birth. Mem Am Anthropol Assoc 1(4):247-300.
4. Klug WS, Cummings MR, Spencer C (2006) Concepts of Genetics (Pearson/Prentice Hall, Upper Saddle River, NJ), 8th Ed.
5. Cunningham FG, et al. (2010) 2010 Williams Obstetrics (McGraw-Hill Medical, New York), 23rd Ed.
6. Tschuprow AA (1915) Zur frage des sinkenden knabenüberschusses unter den ehelich geborenen. Bull l'institut Int Stat 20(2):378-492.
7. Parkes AS (1926) The mammalian sex-ratio. Biol Rev Camb Philos Soc 2(1):1-51.
8. Fisher RA (1930) The Genetical Theory of Natural Selection (Clarendon Press, Oxford).
9. Shettles LB (1964) The great preponderance of human males conceived. Am J Obstet Gynecol 89(1):130-133.
10. McMillen MM (1979) Differential mortality by sex in fetal and neonatal deaths. Science 204(4388):89-91.
11. Pergament E, Toydemir PB, Fiddler M (2002) Sex ratio: A biological perspective of 'Sex and the City'. Reprod Biomed Online 5(1):43-46.
12. Keller CA (1969) Embryonal sex ratios in animals and man. PhD thesis (University of California, Berkeley).
13. Boué A (1976) L'excès de conceptus mâles. La surmortalité des embryons mâles: Réalités ou mythe. Nouv Presse Med 5(20):1307.
14. Creasy MR (1977) The primary sex ratio of man. Ann Hum Biol 4(4):390-392.
15. Degenhardt A, Tholey P, Michaelis H (1980) Primary sex ratio of 125 males to 100 females? Analysis of an artifact. J Hum Evol 9(8):651-654.
16. Boklage CE (2005) The epigenetic environment: Secondary sex ratio depends on differential survival in embryogenesis. Hum Reprod 20(3):583-587.
17. Mikamo K (1969) Female preponderance in the sex ratio during early intrauterine development: A sex chromatin study. Jinrui Idengaku Zasshi 13(4):272-277.
18. Hytten FE, Leitch I (1971) The Physiology of Human Pregnancy (Blackwell Scientific Publications Ltd, Oxford), 2nd Ed.
19. Hassold TJ, et al. (1978) A cytogenetic study of spontaneous abortions in Hawaii. Ann Hum Genet 41(4):443-454.
20. McKeown T, Lowe CR (1951) The sex ratio of stillbirths related to cause and duration of gestation; an investigation of 7,066 stillbirths. Hum Biol 23(1):41-60.
21. Bodmer WF, Edwards AW (1960) Natural selection and the sex ratio. Ann Hum Genet 24(3):239-244.
22. Stevenson AC, Bobrow M (1967) Determinants of sex proportions in man, with consideration of the evidence concerning a contribution from X-linked mutations to intrauterine death. J Med Genet 4(3):190-221.
23. Stirnemann JJ, Samson A, Bernard J-P, Thalabard J-C (2013) Day-specific probabilities of conception in fertile cycles resulting in spontaneous pregnancies. Hum Reprod 28(4):1110-1116.
24. Volpi EV, Bridger JM (2008) FISH glossary: An overview of the fluorescence in situ hybridization technique. Biotechniques 45(4):385-386, 388, 390 passim.
25. Wilton L (2002) Preimplantation genetic diagnosis for aneuploidy screening in early human embryos: A review. Prenat Diagn 22(6):512-518.
26. Munné S, Wells D, Cohen J (2010) Technology requirements for preimplantation genetic diagnosis to improve assisted reproduction outcomes. Fertil Steril 94(2):408-430.
27. Treff NR, et al. (2010) SNP microarray-based 24 chromosome aneuploidy screening is significantly more consistent than FISH. Mol Hum Reprod 16(8):583-589.
28. Hu DG, Guan XY, Hussey N (2007) Gender determination and detection of aneuploidy in single cells using DNA array-based comparative genomic hybridization. Methods Mol Med 132:135-151.
29. Gutiérrez-Mateo C, et al. (2011) Validation of microarray comparative genomic hybridization for comprehensive chromosome analysis of embryos. Fertil Steril 95(3):953-958.
30. Colls P, et al. (2012) Validation of array comparative genome hybridization for diagnosis of translocations in preimplantation human embryos. Reprod Biomed Online 24(6):621-629.
31. Eisenberg B, Wapner RJ (2002) Clinical proceduress in prenatal diagnosis. Best Pract Res Clin Obstet Gynaecol 16(5):611-627.
32. Brambati B, Tului L (2005) Chorionic villus sampling and amniocentesis. Curr Opin Obstet Gynecol 17(2):197-201.
33. MacDorman MF, Munson ML, Kirmeyer S (2007) Fetal and perinatal mortality, United States, 2004. Natl Vital Stat Rep 56(3):1-19.
34. Pinheiro JC, Bates DM (2004) Mixed-Effects Models in S and S-PLUS (Springer, New York).
35. Burnham KP, Anderson DR (2002) Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach (Springer, New York), 2nd Ed.
36. Lukacs PM, et al. (2007) Concerns regarding a call for pluralism of information theory and hypothesis testing. J Appl Ecol 44(2):456-460.
37. Burnham KP, Anderson DR (2004) Multimodel inference: Understanding AIC and BIC in model selection. Sociol Methods Res 33:261-304.
38. Link WA, Barker RJ (2006) Model weights and the foundations of multimodel inference. Ecology 87(10):2626-2635.
39. Bolker BM (2008) Ecological Models and Data in R (Princeton University Press, Princeton).
40. Sakamoto Y, Akaike H (1978) Analysis of cross classified data by AIC. Ann Inst Stat Math 30(1):185-197.
41. Forster MR (2000) Key concepts in model selection: Performance and generalizability. J Math Psychol 44(1):205-231.
42. Mundry R (2011) Issues in information theory-based statistical inference-a commentary from a frequentist's perspective. Behav Ecol Sociobiol 65(1):57-68.
43. Murtaugh PA (2014) In defense of P values. Ecology 95(3):611-617.
44. Barbash-Hazan S, et al. (2009) Preimplantation aneuploid embryos undergo self-correction in correlation with their developmental potential. Fertil Steril 92(3):890-896.
45. Jacobsen R, Møller H, Mouritsen A (1999) Natural variation in the human sex ratio. Hum Reprod 14(12):3120-3125.
46. Ein-Mor E, Mankuta D, Hochner-Celnikier D, Hurwitz A, Haimov-Kochman R (2010) Sex ratio is remarkably constant. Fertil Steril 93(6):1961-1965.
47. Tietze C (1948) A note on the sex ratio of abortions. Hum Biol 20(3):156-160.
48. Stevenson AC (1966) The Sex Chromatin, ed Moore KL (W. B. Saunders, Philadelphia), pp 263-276.
49. Spencer K (2000) The influence of fetal sex in screening for Down syndrome in the second trimester using AFP and free beta-hCG. Prenat Diagn 20(8):648-651.
50. Joseph KS, et al.; (2007) Reconciling the high rates of preterm and postterm birth in the United States. Obstet Gynecol 109(4):813-822.
51. Klebanoff MA (2007) Gestational age: Not always what it seems. Obstet Gynecol 109(4):798-799.
52. Wingate MS, Alexander GR, Buekens P, Vahratian A (2007) Comparison of gestational age classifications: Date of last menstrual period vs. clinical estimate. Ann Epidemiol 17(6):425-430.
53. Tesarík J, Kopecný V, Plachot M, Mandelbaum J (1988) Early morphological signs of embryonic genome expression in human preimplantation development as revealed by quantitative electron microscopy. Dev Biol 128(1):15-20.
54. Ao A, Erickson RP, Winston RM, Handyside AH (1994) Transcription of paternal Y-linked genes in the human zygote as early as the pronucleate stage. Zygote 2(4):281-287.
55. Abdel-Rahman B, Fiddler M, Rappolee D, Pergament E (1995) Expression of transcription regulating genes in human preimplantation embryos. Hum Reprod 10(10):2787-2792.
56. Fiddler M, Abdel-Rahman B, Rappolee DA, Pergament E (1995) Expression of SRY transcripts in preimplantation human embryos. Am J Med Genet 55(1):80-84.
57. Taylor DM, Ray PF, Ao A, Winston RM, Handyside AH (1997) Paternal transcripts for glucose-6-phosphate dehydrogenase and adenosine deaminase are first detectable in the human preimplantation embryo at the three- to four-cell stage. Mol Reprod Dev 48(4):442-448.
58. Monk M, Salpekar A (2001) Expression of imprinted genes in human preimplantation development. Mol Cell Endocrinol 183(Suppl 1):S35-S40.
59. Jeanblanc M, Salvaing J, Mason K, Debey P, Beaujean N (2008) Activation du génome embryonnaire. Gynecol Obstet Fertil 36(11):1126-1132.
60. Gardner DK, Larman MG, Thouas GA (2010) Sex-related physiology of the preimplantation embryo. Mol Hum Reprod 16(8):539-547.
61. Uematsu A, et al. (2002) Parental origin of normal X chromosomes in Turner syndrome patients with various karyotypes: Implications for the mechanism leading to generation of a 45,X karyotype. Am J Med Genet 111(2):134-139.
62. Metzler-Guillemain C, Mignon C, Depetris D, Guichaoua MR, Mattei MG (1999) Bivalent 15 regularly associates with the sex vesicle in normal male meiosis. Chromosome Res 7(5):369-378.
63. Vogt P (1990) Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved "chromatin folding code". Hum Genet 84(4):301-336.
64. Handel MA (2004) The XY body: A specialized meiotic chromatin domain. Exp Cell Res 296(1):57-63.
65. Codina-Pascual M, et al. (2006) Behaviour of human heterochromatic regions during the synapsis of homologous chromosomes. Hum Reprod 21(6):1490-1497.
66. Vergés L, Blanco J, Valero O, Vidal F, Sarrate Z (2014) Chromosome size, morphology, and gene density determine bivalent positioning in metaphase I human spermatocytes. Fertil Steril 101(3):818-824.
67. Stahl A, Hartung M, Devictor M, Bergé-Lefranc JL (1984) The association of the nucleolus and the short arm of acrocentric chromosomes with the XY pair in human spermatocytes: Its possible role in facilitating sex-chromosome acrocentric translocations. Hum Genet 68(2):173-180.
68. Mattei MG, Mattei JF, Ayme S, Giraud F (1982) X-autosome translocations: cytogenetic characteristics and their consequences. Hum Genet 61(4):295-309.
69. Makoff AJ, Flomen RH (2007) Detailed analysis of 15q11-q14 sequence corrects errors and gaps in the public access sequence to fully reveal large segmental duplications at breakpoints for Prader-Willi, Angelman, and inv dup(15) syndromes. Genome Biol 8(6):R114.
70. Bishop MW (1964) Paternal contribution to embryonic death. J Reprod Fertil 7(3):383-396.
71. Suthers G, Smith S, Springbett S (1999) Skewed sex ratios in familial holoprosencephaly and in people with isolated single maxillary central incisor. J Med Genet 36(12):924-926.
72. Keng VW, et al. (2013) Sex bias occurrence of hepatocellular carcinoma in Poly7 molecular subclass is associated with EGFR. Hepatology 57(1):120-130.
73. Griffin DK, Abruzzo MA, Millie EA, Feingold E, Hassold TJ (1996) Sex ratio in normal and disomic sperm: Evidence that the extra chromosome 21 preferentially segregates with the Y chromosome. Am J Hum Genet 59(5):1108-1113.
74. Petersen MB, et al. (1993) Paternal nondisjunction in trisomy 21: Excess of male patients. Hum Mol Genet 2(10):1691-1695.
75. Savage AR, et al. (1998) Elucidating the mechanisms of paternal non-disjunction of chromosome 21 in humans. Hum Mol Genet 7(8):1221-1227.
76. Huether CA, et al. (1996) Sex ratios in fetuses and liveborn infants with autosomal aneuploidy. Am J Med Genet 63(3):492-500.
77. Niedrist D, Riegel M, Achermann J, Rousson V, Schinzel A (2006) Trisomy 18: Changes in sex ratio during intrauterine life. Am J Med Genet A 140(21):2365-2367.
78. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc B 57(1):289-300.
79. Strimmer K (2008) A unified approach to false discovery rate estimation. BMC Bioinformatics 9:303.
80. Hahnemann N (1973) Chromosome studies in induced abortions. Clin Genet 4(4):328-332.
81. Yamamoto M, Ito T, Watanabe GI (1977) Determination of prenatal sex ratio in man. Hum Genet 36(3):265-269.
82. Ohama K (1978) Chromosomal anomalies and sex ratio of induced abortions in early embryogenesis. Acta Obstet Gynaecol Jpn 30(12):1687-1695.
83. Tsuji K, Nakano R (1978) Chromosome studies of embryos from induced abortions in pregnant women age 35 and over. Obstet Gynecol 52(5):542-544.
84. Hoshi N, Yamagami Y, Hanatani K, Tanaka T, Fujimoto S (1990) Chromosomal studies on 934 induced abortuses of middle-aged pregnant women. Asia Oceania J Obstet Gynaecol 16(3):275-281.
85. Hoshi N, Hanatani K, Kishida T, Sagawa T, Fujimoto S (1997) Chromosomal analysis in 894 induced abortuses from women of advanced maternal age in relation to gestational weeks and fetal sex ratio. J Obstet Gynaecol Res 23(1):1-7.
86. Bartels I, Hansmann I, Eiben B (1990) Excess of females in chromosomally normal spontaneous abortuses. Am J Med Genet 35(2):297-298.
87. Guerneri S, et al. (1987) Prevalence and distribution of chromosome abnormalities in a sample of first trimester internal abortions. Hum Reprod 2(8):735-739.
88. Eiben B, et al. (1990) Cytogenetic analysis of 750 spontaneous abortions with the direct-preparation method of chorionic villi and its implications for studying genetic causes of pregnancy wastage. Am J Hum Genet 47(4):656-663.
89. Byrne J, Warburton D (1987) Male excess among anatomically normal fetuses in spontaneous abortions. Am J Med Genet 26(3):605-611.
90. Zeitlin J, et al. (2002) Fetal sex and preterm birth: Are males at greater risk? Hum Reprod 17(10):2762-2768.
91. Ingemarsson I (2003) Gender aspects of preterm birth. BJOG 110(Suppl 20):34-38.
92. James WH (2003) The causes of the excess males among pre-term and post-term births. Hum Reprod 18(3):655-656.
93. Navara KJ (2014) Low gestational weight gain skews human sex ratios towards females. PLoS ONE 9(12):e114304.
94. Lesiński J (1962) Relationship between length of gestation, birth weight and certain other factors. Bull World Health Organ 26(2):183-191.
95. James WH (1994) Cycle day of insemination, sex ratio of offspring and duration of gestation. Ann Hum Biol 21(3):263-266.
96. Veitia RA, Veyrunes F, Bottani S, Birchler JA (2015) X chromosome inactivation and active X upregulation in therian mammals: Facts, questions, and hypotheses. J Mol Cell Biol 7(1):2-11.
97. Ober C, Loisel DA, Gilad Y (2008) Sex-specific genetic architecture of human disease. Nat Rev Genet 9(12):911-922.
98. Cvitic S, et al. (2013) The human placental sexome differs between trophoblast epithelium and villous vessel endothelium. PLoS ONE 8(10):e79233.
99. Buckberry S, Bianco-Miotto T, Bent SJ, Dekker GA, Roberts CT (2014) Integrative transcriptome meta-analysis reveals widespread sex-biased gene expression at the human fetal-maternal interface. Mol Hum Reprod 20(8):810-819.
100. Thornhill AR, Burgoyne PS (1993) A paternally imprinted X chromosome retards the development of the early mouse embryo. Development 118(1):171-174.
101. Minks J, Robinson WP, Brown CJ (2008) A skewed view of X chromosome inactivation. J Clin Invest 118(1):20-23.
102. Yang C, et al. (2011) X-chromosome inactivation: Molecular mechanisms from the human perspective. Hum Genet 130(2):175-185.
103. Desai V, et al. (2011) Favorably skewed X-inactivation accounts for neurological sparing in female carriers of Menkes disease. Clin Genet 79(2):176-182.
104. Brown CJ (1999) Skewed X-chromosome inactivation: Cause or consequence? J Natl Cancer Inst 91(4):304-305.
105. Kristiansen M, et al. (2002) High frequency of skewed X inactivation in young breast cancer patients. J Med Genet 39(1):30-33.
106. Ozbalkan Z, et al. (2005) Skewed X chromosome inactivation in blood cells of women with scleroderma. Arthritis Rheum 52(5):1564-1570.
107. Pegoraro E, et al. (1997) Familial skewed X inactivation: A molecular trait associated with high spontaneous-abortion rate maps to Xq28. Am J Hum Genet 61(1):160-170.
108. Sangha KK, Stephenson MD, Brown CJ, Robinson WP (1999) Extremely skewed X-chromosome inactivation is increased in women with recurrent spontaneous abortion. Am J Hum Genet 65(3):913-917.
109. James WH (2008) Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. J Endocrinol 198(1):3-15.
110. James WH (2008) Further support for the hypothesis that parental hormone levels around the time of conception are associated with human sex ratios at birth. J Biosoc Sci 40(6):855-861.
111. Harlap S (1979) Gender of infants conceived on different days of the menstrual cycle. N Engl J Med 300(26):1445-1448.
112. Wilcox AJ, Weinberg CR, Baird DD (1995) Timing of sexual intercourse in relation to ovulation. Effects on the probability of conception, survival of the pregnancy, and sex of the baby. N Engl J Med 333(23):1517-1521.
113. Spira A, et al. (1993) Biomedical and Demographic Determinants of Reproduction, eds Gray R, Leridon H, Spira A (Oxford Univ Press, New York), pp 271-284.
114. Bernstein ME (1995) Genetic control of the secondary sex ratio. Hum Reprod 10(10):2531-2533.
115. Gray RH, et al. (1998) Sex ratio associated with timing of insemination and length of the follicular phase in planned and unplanned pregnancies during use of natural family planning. Hum Reprod 13(5):1397-1400.
116. Gray RH, et al. (1995) Timing of conception and the risk of spontaneous abortion among pregnancies occurring during the use of natural family planning. Am J Obstet Gynecol 172(5):1567-1572.
117. Krackow S (1995) The developmental asynchrony hypothesis for sex ratio manipulation. J Theor Biol 176(2):273-280.
118. Düsing C (1884) Die Regulierung des Geschlechtsverhältnisses bei der Vermehrung der Menschen, Tiere, und Pflanzen. Jenaische Zeitschrift fur Naturwiss 17:593-940.
119. Charlesworth B (1977) Measuring Selection in Natural Populations, eds Christiansen FB, Fenchel TM (Springer, Berlin), pp 345-363.
120. Hewlett BS (1991) Demography and childcare in preindustrial societies. J Anthropol Res 47(1):1-37.
121. Tuljapurkar S, Steiner UK, Orzack SH (2009) Dynamic heterogeneity in life histories. Ecol Lett 12(1):93-106.
122. Stubblefield JW, Orzack SH (2013) Resource transfers and evolution: Helpful offspring and sex allocation. Theor Popul Biol 83:64-81.