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Evolutionary Biology

, Volume 45, Issue 1, pp 96–104 | Cite as

Maternal Testosterone and Offspring Sex-Ratio in Birds and Mammals: A Meta-Analysis

  • Thomas Merkling
  • Shinichi Nakagawa
  • Malgorzata Lagisz
  • Lisa E. Schwanz
Research Article

Abstract

Sex allocation theory predicts that parents should bias offspring sex to maximize their fitness in a given context. Quantifying the fitness benefits of offspring sex-ratio biases would be facilitated by a better knowledge of their underlying mechanism(s) and associated costs. The hypothesis that steroid hormones are involved in sex determination has gained in popularity recently. Being influenced by external stimuli and involved in a range of physiological processes, they could be a ubiquitous mediator of environmental conditions influencing sex-ratio with low fitness costs. Previous studies indicated that higher maternal testosterone levels led to the overproduction of sons around conception in both birds and mammals. We conducted a systematic review (including meta-analysis) of these studies and, as predicted, we found a weak positive and significant overall effect of maternal testosterone on the proportion of sons. Neither taxa, nor the type of study (experimental/observational), or the timing of timing testosterone manipulation/measure were significant predictors of offspring sex-ratio, which may be explained by low statistical power in addition to low variability between effect sizes. Our meta-analysis provides evidence for a general positive influence of maternal testosterone around conception on the proportion of sons across birds and mammals, although less confidently so for the latter. It begs for more large-scale experimental studies, especially on mammals, and ideally in the wild. It may also have some important consequences for the poultry industry.

Keywords

Differential mortality Poultry Sex ratio Proximate mechanism Sex determination Steroids 

Notes

Acknowledgements

We are grateful to Tom Pike, Dorit Shargil, Joanna Setchell, Lee Koren and Allison Pavitt for responding to requests for additional data. We also thank three anonymous reviewers for useful comments on a previous version of the manuscript. T. M. was supported by an Endeavour Research Fellowship. S. N. is funded by an ARC Future Fellowship (FT130100268).

Data Accessibility

All data and code are available on the Open Science Framework (https://osf.io/67q8d/).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11692_2017_9432_MOESM1_ESM.docx (151 kb)
Supplementary material 1 (DOCX 151 KB)

References

  1. Alonso-Alvarez, C. (2006). Manipulation of primary sex-ratio: An updated review. Avian and Poultry Biology Reviews, 17(1), 1–20.CrossRefGoogle Scholar
  2. Arnon, L., Hazut, N., Tabachnik, T., Weller, A., & Koren, L. (2016). Maternal testosterone and reproductive outcome in a rat model of obesity. Theriogenology, 86(4), 1042–1047.CrossRefPubMedGoogle Scholar
  3. Bartoń, K. (2016). MuMIn: Multi-model inference (version 1.15.6). https://CRAN.R-project.org/package=MuMIn.
  4. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd edn.). Berlin: Springer.Google Scholar
  5. Cameron, E. Z. (2004). Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: Evidence for a mechanism. Proceedings of the Royal Society of London Series B-Biological Sciences, 271(1549), 1723–1728.CrossRefGoogle Scholar
  6. Cameron, E. Z., Lemons, P. R., Bateman, P. W., & Bennett, N. C. (2008). Experimental alteration of litter sex ratios in a mammal. Proceedings of the Royal Society B: Biological Sciences, 275(1632), 323–327.CrossRefPubMedGoogle Scholar
  7. Cameron, E. Z., & Linklater, W. L. (2007). Extreme sex ratio variation in relation to change in condition around conception. Biology Letters, 3(4), 395–397.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cockburn, A., Legge, S., & Double, M. (2002). Sex ratios in birds and mammals: Can the hypotheses be disentangled. In I. C. W. Hardy (Ed.) Sex ratios: Concepts and research methods (pp. 266–286). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  9. Correa, S. M., Horan, C. M., Johnson, P. A., & Adkins-Regan, E. (2011). Copulatory behaviors and body condition predict post-mating female hormone concentrations, fertilization success, and primary sex ratios in Japanese quail. Hormones and Behavior, 59(4), 556–564.CrossRefPubMedGoogle Scholar
  10. Duval, S., & Tweedie, R. (2000). Trim and fill: A simple funnel-plot–based method of testing and adjusting for publication bias in meta-analysis. Biometrics, 56(2), 455–463.CrossRefPubMedGoogle Scholar
  11. Edwards, A. M., & Cameron, E. Z. (2014). Forgotten fathers: Paternal influences on mammalian sex allocation. Trends in Ecology & Evolution, 29(3), 158–164.CrossRefGoogle Scholar
  12. Edwards, A. M., Cameron, E. Z., Pereira, J. C., & Ferguson-Smith, M. A. (2016). Paternal sex allocation: How variable is the sperm sex ratio? Journal of Zoology, 299(1), 37–41.CrossRefGoogle Scholar
  13. Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629–634.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Fuertbauer, I., Heistermann, M., Schuelke, O., & Ostner, J. (2012). Brief communication: Fecal androgen excretion and fetal sex effects during gestation in wild assamese macaques (Macaca assamensis). American Journal of Physical Anthropology, 147(2), 334–339. doi: 10.1002/ajpa.21646.CrossRefGoogle Scholar
  15. Gam, A. E., Mendonça, M. T., & Navara, K. J. (2011). Acute corticosterone treatment prior to ovulation biases offspring sex ratios towards males in zebra finches Taeniopygia guttata. Journal of Avian Biology, 42(3), 253–258.CrossRefGoogle Scholar
  16. Gleason, E. D., Fuxjager, M. J., Oyegbile, T. O., & Marler, C. A. (2009). Testosterone release and social context: When it occurs and why. Frontiers in Neuroendocrinology, 30(4), 460–469.CrossRefPubMedGoogle Scholar
  17. Goerlich, V. C., Dijkstra, C., Boonekamp, J. J., & Groothuis, T. G. G. (2010). Change in body mass can overrule the effects of maternal testosterone on primary offspring sex ratio of first eggs in homing pigeons. Physiological and Biochemical Zoology, 83(3), 490–500.CrossRefPubMedGoogle Scholar
  18. Goerlich, V. C., Dijkstra, C., Schaafsma, S. M., & Groothuis, T. G. G. (2009). Testosterone has a long-term effect on primary sex ratio of first eggs in pigeons-in search of a mechanism. General and Comparative Endocrinology, 163(1–2), 184–192.CrossRefPubMedGoogle Scholar
  19. Grant, V. J. (2007). Could maternal testosterone levels govern mammalian sex ratio deviations? Journal of Theoretical Biology, 246(4), 708–719.CrossRefPubMedGoogle Scholar
  20. Grant, V. J., & Chamley, L. W. (2010). Can mammalian mothers influence the sex of their offspring peri-conceptually? Reproduction (Cambridge, England), 140(3), 425–433.CrossRefGoogle Scholar
  21. Grant, V. J., Irwin, R. J., Standley, N. T., Shelling, A. N., & Chamley, L. W. (2008). Sex of Bovine Embryos May Be Related to Mothers’ Preovulatory Follicular Testosterone. Biology of Reproduction, 78(5), 812–815.CrossRefPubMedGoogle Scholar
  22. Grant, V. J., Konecna, M., Sonnweber, R.-S., Irwin, R. J., & Wallner, B. (2011). Macaque mothers’ preconception testosterone levels relate to dominance and to sex of offspring. Animal Behaviour, 82(4), 893–899.CrossRefGoogle Scholar
  23. Hedges, L. V., & Olkin, I. (2014). Statistical methods for meta-analysis. New York: Academic press.Google Scholar
  24. Helle, S., Laaksonen, T., Adamsson, A., Paranko, J., & Huitu, O. (2008). Female field voles with high testosterone and glucose levels produce male-biased litters. Animal Behaviour, 75(3), 1031–1039.CrossRefGoogle Scholar
  25. Higgins, J. P., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557–560.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Ihle, M., Winney, I. S., Krystalli, A., & Croucher, M. (2017). Striving for transparent and credible research: Practical guidelines for behavioral ecologists. Behavioral Ecology, 28(2), 348–354.CrossRefGoogle Scholar
  27. Jennions, M. D., & Møller, A. P. (2002). Relationships fade with time: A meta-analysis of temporal trends in publication in ecology and evolution. Proceedings of the Royal Society of London B: Biological Sciences, 269(1486), 43–48.CrossRefGoogle Scholar
  28. Kesler, D. J., Favero, R. J., Esarey, J. C., & Berger, L. L. (1995). Controlled delivery of testosterone propionate suppresses fertility in treated females and induces prenatal androgenization in female offspring without phenotypic masculinization. Drug Development and Industrial Pharmacy, 21(13), 1513–1527.CrossRefGoogle Scholar
  29. Komdeur, J. (2012). Sex allocation. In N. J. Royle, P. T. Smiseth & M. Kölliker (Eds.) The evolution of parental care (pp. 171–188). Oxford: Oxford University Press.CrossRefGoogle Scholar
  30. Komdeur, J., Magrath, M. J. L., & Krackow, S. (2002). Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proceedings of the Royal Society of London Series B-Biological Sciences, 269(1495), 1067–1072.CrossRefGoogle Scholar
  31. Komdeur, J., & Pen, I. (2002). Adaptive sex allocation in birds: The complexities of linking theory and practice. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 357(1419), 373–380.CrossRefGoogle Scholar
  32. Krackow, S. (1995). Potential mechanisms for sex ratio adjustment in mammals and birds. Biological Reviews, 70(2), 225–241.CrossRefPubMedGoogle Scholar
  33. Lovern, M. B., & Wade, J. (2003). Yolk testosterone varies with sex in eggs of the lizard, Anolis carolinensis. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 295(2), 206–210.CrossRefGoogle Scholar
  34. Malo, A. F., Martinez-Pastor, F., Garcia-Gonzalez, F., Garde, J., Ballou, J. D., & Lacy, R. C. (2017). A father effect explains sex-ratio bias. Proceedings of the Royal Society of London Series B-Biological Sciences, 284(1861), 20171159.CrossRefGoogle Scholar
  35. Mazuc, J., Bonneaud, C., Chastel, O., & Sorci, G. (2003). Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecology Letters, 6(12), 1084–1090.CrossRefGoogle Scholar
  36. Michonneau, F., Brown, J. W., & Winter, D. J. (2016). rotl: An R package to interact with the Open Tree of Life data. Methods in Ecology and Evolution, 7(12), 1476–1481.CrossRefGoogle Scholar
  37. Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Annals of Internal Medicine, 151(4), 264–269.CrossRefPubMedGoogle Scholar
  38. Navara, K. J. (2010). Programming of offspring sex ratios by maternal stress in humans: Assessment of physiological mechanisms using a comparative approach. Journal of Comparative Physiology B, 180(6), 785–796.CrossRefGoogle Scholar
  39. Navara, K. J. (2013a). Hormone-mediated adjustment of sex ratio in vertebrates. Integrative and Comparative Biology, 53(6), 877–887.CrossRefPubMedGoogle Scholar
  40. Navara, K. J. (2013b). The role of steroid hormones in the adjustment of primary sex ratio in birds: Compiling the pieces of the puzzle. Integrative and comparative biology, 53(6), 923–937.CrossRefPubMedGoogle Scholar
  41. Pandian, T. J., & Sheela, S. G. (1995). Hormonal induction of sex reversal in fish. Aquaculture, 138(1), 1–22.CrossRefGoogle Scholar
  42. Parker, T. H., Forstmeier, W., Koricheva, J., Fidler, F., Hadfield, J. D., Chee, Y. E., et al. (2016). Transparency in ecology and evolution: Real problems, real solutions. Trends in Ecology & Evolution, 31(9), 711–719.CrossRefGoogle Scholar
  43. Pavitt, A. T., Pemberton, J. M., Kruuk, L. E. B., & Walling, C. A. (2016). Testosterone and cortisol concentrations vary with reproductive status in wild female red deer. Ecology and Evolution, 6(4), 1163–1172.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pike, T. W., & Petrie, M. (2005). Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Animal Behaviour, 70(4), 745–751.CrossRefGoogle Scholar
  45. Pike, T. W., & Petrie, M. (2006). Experimental evidence that corticosterone affects offspring sex ratios in quail. Proceedings Biological sciences/The Royal Society, 273(1590), 1093–1098.CrossRefGoogle Scholar
  46. Pinson, S. E., Parr, C. M., Wilson, J. L., & Navara, K. J. (2011a). Acute corticosterone administration during meiotic segregation stimulates females to produce more male offspring. Physiological and Biochemical Zoology, 84(3), 292–298.CrossRefPubMedGoogle Scholar
  47. Pinson, S. E., Wilson, J. L., & Navara, K. J. (2011b). Elevated testosterone during meiotic segregation stimulates laying hens to produce more sons than daughters. General and Comparative Endocrinology, 174(2), 195–201.CrossRefPubMedGoogle Scholar
  48. Pinson, S. E., Wilson, J. L., & Navara, K. J. (2015). Timing matters: Corticosterone injections 4 h before ovulation bias sex ratios towards females in chickens. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 185(5), 539–546.CrossRefGoogle Scholar
  49. R Core Team. (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.
  50. Robert, K. A., & Schwanz, L. E. (2011). Emerging sex allocation research in mammals: Marsupials and the pouch advantage. Mammal Review, 41(1), 1–22.CrossRefGoogle Scholar
  51. Rutkowska, J., & Badyaev, A. V. (2008). Meiotic drive and sex determination: Molecular and cytological mechanisms of sex ratio adjustment in birds. Philosophical Transactions of the Royal Society B-Biological Sciences, 363(1497), 1675–1686.CrossRefGoogle Scholar
  52. Rutkowska, J., & Cichoń, M. (2006). Maternal testosterone affects the primary sex ratio and offspring survival in zebra finches. Animal Behaviour, 71(6), 1283–1288.CrossRefGoogle Scholar
  53. Senior, A. M., Grueber, C. E., Kamiya, T., Lagisz, M., O’Dwyer, K., Santos, E. S., & Nakagawa, S. (2016). Heterogeneity in ecological and evolutionary meta-analyses: Its magnitude and implications. Ecology, 97(12), 3293–3299.CrossRefPubMedGoogle Scholar
  54. Setchell, J. M., Smith, T. E., & Knapp, L. A. (2015). Androgens in a female primate: Relationships with reproductive status, age, dominance rank, fetal sex and secondary sexual color. Physiology & Behavior, 147, 245–254.CrossRefGoogle Scholar
  55. Shargal, D., Shore, L., Roteri, N., Terkel, A., Zorovsky, Y., Shemesh, A., & Steinberger, Y. (2008). Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring. Theriogenology, 69(6), 673–680.CrossRefPubMedGoogle Scholar
  56. Uller, T., & Badyaev, A. V. (2009). Evolution of “determinants” in sex-determination: A novel hypothesis for the origin of environmental contingencies in avian sex-bias. Seminars in Cell & Developmental Biology, 20(3), 304–312.CrossRefGoogle Scholar
  57. Veiga, J. P., Vinuela, J., Cordero, P. J., Aparicio, J. M., & Polo, V. (2004). Experimentally increased testosterone affects social rank and primary sex ratio in the spotless starling. Hormones and Behavior, 46(1), 47–53.CrossRefPubMedGoogle Scholar
  58. Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3), 1–48.CrossRefGoogle Scholar
  59. Wallace, B. C., Small, K., Brodley, C. E., Lau, J., & Trikalinos, T. A. (2012). Deploying an interactive machine learning system in an evidence-based practice center: Abstrackr. In Proceedings of the 2nd ACM SIGHIT International Health Informatics Symposium (pp. 819–824). Miami: ACM. http://dl.acm.org/citation.cfm?id=2110464.
  60. West, S. A. (2009). Sex allocation. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
  61. West, S. A., & Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295(5560), 1685–1688.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.School of Biological, Earth and Environmental Sciences, Evolution & Ecology Research CentreUniversity of New South WalesSydneyAustralia

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