Evolutionary Biology

, Volume 36, Issue 2, pp 190–200

Trends in Population Sex Ratios May be Explained by Changes in the Frequencies of Polymorphic Alleles of a Sex Ratio Gene

Research Article

Abstract

A test for heritability of the sex ratio in human genealogical data is reported here, with the finding that there is significant heritability of the parental sex ratio by male, but not female offspring. A population genetic model was used to examine the hypothesis that this is the result of an autosomal gene with polymorphic alleles, which affects the sex ratio of offspring through the male reproductive system. The model simulations show that an equilibrium sex ratio may be maintained by frequency dependent selection acting on the heritable variation provided by the gene. It is also shown that increased mortality of pre-reproductive males causes an increase in male births in following generations, which explains why increases in the sex ratio have been seen after wars, also why higher infant and juvenile mortality of males may be the cause of the male-bias typically seen in the human primary sex ratio. It is concluded that various trends seen in population sex ratios are the result of changes in the relative frequencies of the polymorphic alleles of the proposed gene. It is argued that this occurs by common inheritance and that parental resource expenditure per sex of offspring is not a factor in the heritability of sex ratio variation.

Keywords

Sex ratio Heritable variation Human genetics Polymorphism Mortality War 

References

  1. Ancestry.com. (2008). British Army WWI Service Records, 1914–1920 [online database]. The Generations Network, Inc., Provo, UT, USA. http://www.ancestry.co.uk. Accessed 29 Oct 2008.
  2. Beladjal, L., Vandekerckhove, T. T. M., Muyssen, B., Heyrman, J., de Caesemaeker, J., & Mertens, J. (2002). B-chromosomes and male-biased sex ratio with paternal inheritance in the fairy shrimp Branchipus schaefferi (Crustacea, Anostraca). Heredity, 88, 356–360. doi:10.1038/sj.hdy.6800061.PubMedCrossRefGoogle Scholar
  3. Bibbins, P. E., Lipshultz, L. I., Ward, J. B., & Legator, M. S. (1988). Fluorescent body distribution in spermatozoa in the male with exclusively female offspring. Fertility and Sterility, 49(4), 670–675.PubMedGoogle Scholar
  4. Chandler, J. E., Steinholt-Chenevert, H. C., Adkinson, R. W., & Moser, E. B. (1998). Sex ratio variation between ejaculates within sire evaluated by polymerase chain reaction, calving, and farrowing records. Journal of Dairy Science, 81(7), 1855–1867.PubMedCrossRefGoogle Scholar
  5. Charnov, E. L. (1982). The theory of sex allocation. Princeton, NJ: Princeton University Press.Google Scholar
  6. Curtsinger, J. W., Ito, R., & Hiraizumi, Y. (1983). A 2-Generation study of human sex-ratio variation. American Journal of Human Genetics, 35(5), 951–961.PubMedGoogle Scholar
  7. Darwin, C. 1871. The Descent of Man. London: Murray.Google Scholar
  8. Denny, K. (2008). Big and tall parents do not have more sons. Journal of Theoretical Biology, 250(4), 752–753. doi:10.1016/j.jtbi.2007.11.004.PubMedCrossRefGoogle Scholar
  9. Dmowski, W. P., Gaynor, L., Rao, R., Lawrence, M., & Scommegna, A. (1979). Use of albumin gradients for X-sperm and Y-sperm separation and clinical experience with male sex preselection. Fertility and Sterility, 31(1), 52–57.PubMedGoogle Scholar
  10. Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Oxford University Press.Google Scholar
  11. Fuster, C., Rigola, M. A., & Egozcue, J. (2004). Human supernumeraries: Are they B chromosomes? Cytogenetic and Genome Research, 106(2–4), 165–172. doi:10.1159/000079283.PubMedCrossRefGoogle Scholar
  12. Gelman, A. (2007). Letter to the editors regarding some papers of Dr. Satoshi Kanazawa. Journal of Theoretical Biology, 245(3), 597–599. doi:10.1016/j.jtbi.2006.11.005.PubMedCrossRefGoogle Scholar
  13. GenealogyForum.com. (2008). Genealogy Forum GEDCOM Library. Golden Gate Services, Inc., Armada, Michigan. http://www.genealogyforum.com/gedcom. Accessed 29 Oct 2008.
  14. Gini, C. (1908). Il Sesso dal Punto di Vista Statistico. Milan: Sandron.Google Scholar
  15. Gini, C. (1955). Sulla probabilita che x termini di una serie erratica sieno tutti crescenti (o non decrescenti) ovvero tutti decrescenti (o non crescenti) con applicazioni ai rapporti dei sessi nelle nascite umane in intervalli successivi e alle disposizioni sessi nelle fratellanze umane. Metron, 17(3–4), 1–41.Google Scholar
  16. Graffelman, J., Fugger, E. F., Keyvanfar, K., & Schulman, J. D. (1999). Human live birth and sperm-sex ratios compared. Human Reproduction (Oxford, England), 14(11), 2917–2919. doi:10.1093/humrep/14.11.2917.CrossRefGoogle Scholar
  17. Graffelman, J., & Hoekstra, R. F. (2000). A statistical analysis of the effect of warfare on the human secondary sex ratio. Human Biology, 72(3), 433–445.Google Scholar
  18. Gray, R. H., Simpson, J. L., Bitto, A. C., Queenan, J. T., Li, C. J., Kambic, R. T., 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. Human Reproduction (Oxford, England), 13(5), 1397–1400. doi:10.1093/humrep/13.5.1397.CrossRefGoogle Scholar
  19. Harlap, S. (1979). Gender of infants conceived on different days of the menstrual-cycle. The New England Journal of Medicine, 300(26), 1445–1448.PubMedCrossRefGoogle Scholar
  20. Irving, J., Bittles, A., Peverall, J., Murch, A., & Matson, P. (1999). The ratio of X- and Y-bearing sperm in ejaculates of men with three or more children of the same sex. Journal of Assisted Reproduction and Genetics, 16(9), 492–494. doi:10.1023/A:1020555101059.PubMedCrossRefGoogle Scholar
  21. Jacobsen, R., Møller, H., & Mouritsen, A. (1999). Natural variation in the human sex ratio. Human Reproduction (Oxford, England), 14(12), 3120–3125. doi:10.1093/humrep/14.12.3120.CrossRefGoogle Scholar
  22. James, W. H. (1971). Cycle day of insemination, coital rate, and sex ratio. Lancet, 297(7690), 112–114. doi:10.1016/S0140-6736(71)90844-0.CrossRefGoogle Scholar
  23. James, W. H. (1995). What stabilizes the sex-ratio. Annals of Human Genetics, 59, 243–249. doi:10.1111/j.1469-1809.1995.tb00744.x.PubMedCrossRefGoogle Scholar
  24. James, W. H. (2000). Analysing data on the sex ratio of human births by cycle day of conception. Human Reproduction (Oxford, England), 15(5), 1206–1207. doi:10.1093/humrep/15.5.1206.CrossRefGoogle Scholar
  25. James, W. H., & Rostron, J. (1985). Parental age, parity and sex-ratio in births in England and Wales, 1968–1977. Journal of Biosocial Science, 17(1), 47–56. doi:10.1017/S0021932000015467.PubMedCrossRefGoogle Scholar
  26. Kanazawa, S. (2005). Big and tall parents have more sons: Further generalizations of the Trivers-Willard hypothesis. Journal of Theoretical Biology, 235(4), 583–590. doi:10.1016/j.jtbi.2005.02.010.PubMedCrossRefGoogle Scholar
  27. Kanazawa, S. (2007). Big and tall soldiers are more likely to survive battle: a possible explanation for the ‘returning soldier effect’ on the secondary sex ratio. Human Reproduction (Oxford, England), 22, 3002–3008. doi:10.1093/humrep/dem239.CrossRefGoogle Scholar
  28. Khoury, M. J., Erickson, J. D., & James, L. M. (1984). Paternal effects on the human sex-ratio at birth––evidence from interracial crosses. American Journal of Human Genetics, 36(5), 1103–1111.PubMedGoogle Scholar
  29. Morton, N. E., Chung, C. S., & Mi, M. P. (1967). Genetics of interracial crosses in Hawaii. Monographs in Human Genetics, 3, 1–158.PubMedGoogle Scholar
  30. Parazzini, F., La Vecchia, C., Levi, F., & Franceschi, S. (1998). Trends in male: Female ratio among newborn infants in 29 countries from five continents. Human Reproduction (Oxford, England), 13(5), 1394–1396. doi:10.1093/humrep/13.5.1394.CrossRefGoogle Scholar
  31. Perez, A., Eger, R., Domenichini, V., Kambic, R., & Gray, R. H. (1985). Sex-ratio associated with natural family-planning. Fertility and Sterility, 43(1), 152–153.PubMedGoogle Scholar
  32. Pomiankowski, A., & Hurst, L. D. (1999). Driving sexual preference. Trends in Ecology and Evolution, 14(11), 425–426. doi:10.1016/S0169-5347(99)01701-2.PubMedCrossRefGoogle Scholar
  33. Premoli, M. C., Sella, G., & Berra, G. P. (1996). Heritable variation of sex ratio in a polychaete worm. Journal of Evolutionary Biology, 9(6), 845–854. doi:10.1046/j.1420-9101.1996.9060845.x.CrossRefGoogle Scholar
  34. Ruder, A. (1985). Paternal-age and birth-order effect on the human secondary sex-ratio. American Journal of Human Genetics, 37(2), 362–372.PubMedGoogle Scholar
  35. Seger, J., & Stubblefield, J. W. (2002). Models of sex ratio evolution. In I. C. W. Hardy (Ed.), Sex ratios concepts and research methods (pp. 2–25). Cambridge, MA: Cambridge University Press.Google Scholar
  36. Shaw, R. F., & Mohler, J. D. (1953). The selective significance of the sex ratio. American Naturalist, 87, 337–342. doi:10.1086/281794.CrossRefGoogle Scholar
  37. Trichopoulos, D. (1967). Evidence of genetic variation in the human sex ratio. Human Biology, 39(2), 170–175.Google Scholar
  38. Uchmanski, J., & Grimm, V. (1996). Individual-based modelling in ecology: What makes the difference? Trends in Ecology and Evolution, 11(10), 437–441. doi:10.1016/0169-5347(96)20091-6.CrossRefGoogle Scholar
  39. Voordouw, M. J., Robinson, H. E., & Anholt, B. R. (2005). Paternal inheritance of the primary sex ratio in a copepod. Journal of Evolutionary Biology, 18(5), 1304–1314. doi:10.1111/j.1420-9101.2005.00922.x.PubMedCrossRefGoogle Scholar
  40. Wilcox, A. J., Weinberg, C. R., & Baird, D. D. (1995). Timing of sexual intercourse in relation to ovulation––effects on the probability of conception, survival of the pregnancy, and sex of the baby. The New England Journal of Medicine, 333(23), 1517–1521. doi:10.1056/NEJM199512073332301.PubMedCrossRefGoogle Scholar
  41. Yusa, Y., & Suzuki, Y. (2003). A snail with unbiased population sex ratios but highly biased brood sex ratios. Proceedings of the Royal Society of London Biological Science Series B, 270(1512), 283–288. doi:10.1098/rspb.2002.2226.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Evolutionary Biology GroupNewcastle UniversityNewcastle upon TyneUK

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