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PARTIALLY CONSTRAINED SEX ALLOCATION AND THE INDIRECT EFFECTS OF ASSISTED REPRODUCTIVE TECHNOLOGIES ON THE HUMAN SEX RATIO

Published online by Cambridge University Press:  19 April 2016

Ian C. W. Hardy*
Affiliation:
School of Biosciences, University of Nottingham, UK
Walid E. Maalouf
Affiliation:
Division of Child Heath, Obstetrics and Gynaecology, Queen’s Medical Centre, University of Nottingham, UK
*
1Corresponding author. Email: [email protected]

Summary

Infertility affects around 15% of human couples and in many countries approximately 1–4% of babies are born following Assisted Reproductive Technologies (ART). Several ART techniques are used and these differentially affect the sex ratio of offspring successfully produced. These direct effects on sex ratio also have the potential to influence, indirectly, the sex ratios of offspring born to untreated couples. This is of concern because human sex ratio bias may adversely affect public health. Here the extent of indirect effects of ART that could operate, via Fisherian frequency-dependent natural selection, on the progeny sex ratio of unassisted members of a population is heuristically modelled. Given the degrees to which ART techniques bias sex ratios directly, it is predicted that well over 20% of couples would have to reproduce via ART for there to be any discernible effect on the sex ratios produced, in response, by the remainder of the population. This value is greater than the estimated prevalence of infertility problems among human couples. It is concluded that providing ART to couples with fertility problems does not currently generate significant ethical issues or public health concern in terms of indirect effects on the offspring sex ratios of untreated couples.

Type
Research Article
Copyright
Copyright © Cambridge University Press, 2016 

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References

Almond, D. & Edlund, L. (2007) Trivers–Willard at birth and one year: evidence from US natality data 1983–2001. Proceedings of the Royal Society of London B 274, 24912496.Google Scholar
Almond, D. & Edlund, L. (2008) Son-biased sex ratios in the 2000 United States Census. Proceedings of the National Academy of Sciences of the USA 105, 56815682.Google Scholar
Argasinki, K. (2013) The dynamics of sex ratio evolution: from the gene perspective to multi-level selection. PLOS One 8(4), e60405.Google Scholar
Bereczkei, T. & Dunbar, R. I. M. (1997) Female-biased reproductive strategies in a Hungarian Gypsy population. Proceedings of the Royal Society of London B 264, 1722.CrossRefGoogle Scholar
Bhattacharya, P. C. (2013) Gender inequality and the sex ratio in three emerging economies. Progress in Development Studies 13, 117133.Google Scholar
Bull, J. J. & Charnov, E. L. (1988) How fundamental are Fisherian sex ratios? Oxford Surveys in Evolutionary Biology 5, 98135.Google Scholar
Chang, H. J., Lee, J. R., Jee, B. C., Suh, C. S. & Kim, S. H. (2009) Impact of blastocyst transfer on offspring sex ratio and the monozygotic twinning rate: a systematic review and meta-analysis. Fertility and Sterility 91, 23812390.Google Scholar
Chevrier, C. & Bressac, C. (2002) Sperm storage and use after multiple mating in Dinarmus basalis (Hymenoptera: Pteromalidae). Journal of Insect Behaviour 15, 385398.Google Scholar
Chipman, A. & Morrison, E. (2013) The impact of sex ratio and economic status on local birth rates. Biology Letters 9, 20130027.Google Scholar
de Mouzon, J. (2008) ICMART. Preliminary IVF World Results . ESHRE, Barcelona.Google Scholar
Dean, J. H., Chapman, M. G. & Sullivan, E. A. (2010) The effect on human sex ratio at birth by assisted reproductive technology (ART) procedures – an assessment of babies born following single embryo transfers, Australia and New Zealand, 2002–2006. BJOG: An International Journal of Obstetrics and Gynaecology 117, 16281634.Google Scholar
Fedder, J., Loft, A., Parner, E. T., Rasmussen, S. & Pinborg, A. (2013) Neonatal outcome and congenital malformations in children born after ICSI with testicular or epididymal sperm: a controlled national cohort study. Human Reproduction 28, 230240.Google Scholar
Fisher, R. A. (1930) The Genetical Theory of Natural Selection. Clarendon Press, Oxford.Google Scholar
Frank, S. A. (2002) A touchstone in the study of adaptation. Evolution 56, 25612564.Google Scholar
Gardner, A. (2014) Dynamics of sex ratio and female unmatedness under haplodiploidy. Ecology and Evolution 4, 16231628.Google Scholar
Godfray, H. C. J. (1990) The causes and consequences of constrained sex allocation in haplodiploid animals. Journal of Evolutionary Biology 3, 317.Google Scholar
Guilmoto, C. Z. (2015) The masculinization of births: overview and current knowledge. Population-E 70, 183244.Google Scholar
Helle, T., Kaar, P., Helama, S. & Jokela, J. (2008) Do humans adjust offspring sex according to the local operational sex ratio? Evolutionary Ecology Research 10, 775785.Google Scholar
Hesketh, T. & Min, J. M. (2012) The effects of artificial gender imbalance. EMBO Reports 13, 487492.Google Scholar
Hesketh, T. & Xing, Z. W. (2006) Abnormal sex ratios in human populations: causes and consequences. Proceedings of the Natural Academy of Sciences of the USA 103, 1327113275.Google Scholar
Hesketh, T., Lu, L. & Xing, Z. W. (2011) The consequences of son preference and sex-selective abortion in China and other Asian countries. Canadian Medical Association Journal 183, 13741377.CrossRefGoogle Scholar
HFEA (2009) Long-Term Data – Birth Rates. URL: http://www.hfea.gov.uk/2588.html.Google Scholar
James, W. H. (2000) Secular movements in sex ratios of adults and of births in populations during the past half-century. Human Reproduction 15, 11781183.Google Scholar
James, W. H. (2011) Notes towards an explanation of the reported effect of mammalian breeding systems on offspring sex ratio. Laboratory Animals 45, 286.Google Scholar
James, W. H. (2012) The relevance of the epidemiology of human sex ratios at birth to some medical problems. Paediatric and Perinatal Epidemiology 26, 181189.CrossRefGoogle ScholarPubMed
James, W. H. (2013) Evolution and the variation of mammalian sex ratios at birth: reflections on Trivers and Willard (1973). Journal of Theoretical Biology 334, 141148.CrossRefGoogle ScholarPubMed
Lazarus, J. (2002) Human sex ratios: adaptations and mechanisms, problems and prospects. In Hardy, I. C. W. (ed) Sex Ratios: Concepts and Research Methods. Cambridge University Press, Cambridge, pp. 12871311.Google Scholar
Lummaa, V., Merila, J. & Kause, A. (1998) Adaptive sex ratio variation in pre-industrial human (Homo sapiens) populations? Proceedings of the Royal Society of London B 265, 563568.Google Scholar
Luna, M., Duke, M., Copperman, A., Grunfeld, L., Sandler, B. & Barritt, J. (2007) Blastocyst embryo transfer is associated with a sex–ratio imbalance in favor of male offspring. Fertility and Sterility 87, 519523.Google Scholar
Maalouf, W. E., Mincheva, M. N., Campbell, B. K. & Hardy, I. C. W. (2014) Effects of assisted reproductive technologies on human sex ratio at birth. Fertility and Sterility 101, 13211325.Google Scholar
Mace, R. & Jordan, F. (2005) The evolution of human sex ratio at birth: a bio-cultural analysis. In Mace, R., Holden, C. J. & Shennan, S. (eds) The Evolution of Cultural Diversity: A Phylogenetic Approach. University College London Press, London, pp. 207216.Google Scholar
Mackenzie, C. A., Lockridge, A. & Keith, M. (2005) Declining sex ratio in a first nation community. Environmental Health Perspectives 113, 12951298.Google Scholar
Madan, K. & Breuning, M. H. (2014) Impact of prenatal technologies on the sex ratio in India: an overview. Genetics in Medicine 16, 425432.Google Scholar
Menezo, Y. J., Chouteau, J., Torello, J., Girard, A. & Veiga, A. (1999) Birth weight and sex ratio after transfer at the blastocyst stage in humans. Fertility and Sterility 72, 221224.Google Scholar
Moss, J. H. & Maner, J. K. (2016) Biased sex ratios influence fundamental aspects of Human mating. Personality and Social Psychology Bulletin 42, 7280.Google Scholar
Murakami, M., Egasghira, A., Tanaka, K., Mine, C., Otsubo, H. & Kuramoto, T. (2014) Perinatal outcomes for transfer of blastocysts vitrified and warmed in defined solutions with recombinant human albumin: 374 babies born after 898 embryo transfers. Journal of Assisted Reproduction Genetics 31, 16051610.CrossRefGoogle ScholarPubMed
NICE (2004) Fertility: Assessment and Treatment for People with Fertility Problems. RCOG Press, UK.Google Scholar
ONS (2011) Birth Summary Tables – England and Wales, 2011 (Final). Office for National Statistics.Google Scholar
Orzack, S. H., Stubblefield, J. W., Akmaev, V. R., Colls, R., Munné, T. S., Steinsaltz, D. & Zuckerman, J. E. (2016) The human sex ratio from conception to birth. Proceedings of the National Academy of Sciences of the USA doi: 10.1073/pnas.1416546112.Google Scholar
Pyeritz, R. E. (1998) Sex: what we make of it. Journal of the American Medical Association 279, 269279.Google Scholar
Ranta, E., Lummaa, V., Veijo, K. & Merila, J. (2000) Dynamics of adaptive sex ratios. Ecology Letters 3, 3034.Google Scholar
Seger, J. & Stubblefield, J. W. (2002) Models of sex ratio evolution. In Hardy, I. C. W. (ed.) Sex Ratios: Concepts and Research Methods. Cambridge University Press, Cambridge, pp. 225.Google Scholar
Setti, A. S., Figueira, R. C., Braga, D. P., Iaconelli, A. Jr & Borges, E. Jr (2012) Gender incidence of intracytoplasmic morphologically selected sperm injection-derived embryos: a prospective randomized study. Reproductive BioMedicine Online 24, 420423.Google Scholar
Shrivastava, S. R., Shrivastava, P. S. & Ramasamy, J. (2014) Public health interventions to stabilize the asymmetrical sex ratio in India. Biology and Medicine 7, 2 1000e115.Google Scholar
Shrivastava, S. R., Shrivastava, P. S. & Ramasamy, J. (2015) Preparing against the challenge of skewed sex ratio: Indian perspective. International Journal of Analytical, Pharmaceutical and Biomedical Sciences 4, 1113.Google Scholar
Song, S. G. (2014) Evidence of adaptive intergenerational sex ratio adjustment in contemporary human populations. Theoretical Population Biology 92, 1421.CrossRefGoogle ScholarPubMed
Tarin, J. J., Bernabeu, R., Baviera, A., Bonada, M. & Cano, A. (1995) Sex selection may be inadvertently performed in in-vitro fertilization–embryo transfer programmes. Human Reproduction 10, 29922998.Google Scholar
Tarin, J. J., García-Pérez, M. A., Hermengildo, C. & Cano, A. (2014) Changes in sex ratio from fertilization to birth in assisted-reproductive-treatment cycles. Reproductive Biology and Endocrinology 12, 56.Google Scholar
Tucker, J. D., Henderson, G. E., Wang, T. F., Huang, Y. Y., Parish, W., Pan, S. M. et al. (2005) Surplus men, sex work and the spread of HIV in China. AIDS 19, 539547.Google Scholar
Werren, J. H. & Charnov, E. L. (1978) Facultative sex ratios and population dynamics. Nature 272, 349350.Google Scholar
West, S. A. (2009) Sex Allocation. Princeton University Press, Princeton.Google Scholar
West, S. A. & Burton-Chellew, M. N. (2013) Human behavioral ecology. Behavioral Ecology 24, 10431045.Google Scholar
Zhou, C., Wang, X. L., Zheng, W. J., Zhou, X. D., Li, L. & Hesketh, T. (2012a) The high sex ratio in China: what do the Chinese think? Journal of Biosocial Science 44, 121125.Google Scholar
Zhou, C., Wang, X. L., Zhou, X. D. & Hesketh, T. (2012b) Son preference and sex-selective abortion in China: informing policy option. International Journal of Public Health 57, 459465.Google Scholar
Zhou, C., Zhou, X. D., Wang, X. L., Zheng, W. J. & Hesketh, T. (2013) Changing gender preferences in China today: implications for the sex ratio. Indian Journal of Gender Studies 20, 5168.Google Scholar
Zhou, X. D., Wang, X. L., Li, L. & Hesketh, T. (2011) The very high sex ratio in rural China: impact on the psychosocial wellbeing of unmarried men. Social Science & Medicine 73, 14221427.Google Scholar
Zhou, X., Yan, Z. & Hesketh, T. (2012c) Depression and aggression in never-married men in China: a growing problem. Social Psychiatry and Psychiatric Epidemiology 48, 10871093.CrossRefGoogle Scholar
Zhu, J., Zhuang, X., Chen, L., Liu, P. & Qiao, J. (2015) Effect of embryo culture media on percentage of males at birth. Human Reproduction 10, 17.Google Scholar