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.
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References
Alonso-Alvarez, C. (2006). Manipulation of primary sex-ratio: An updated review. Avian and Poultry Biology Reviews, 17(1), 1–20.
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.
Bartoń, K. (2016). MuMIn: Multi-model inference (version 1.15.6). https://CRAN.R-project.org/package=MuMIn.
Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd edn.). Berlin: Springer.
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.
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.
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.
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.
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.
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.
Edwards, A. M., & Cameron, E. Z. (2014). Forgotten fathers: Paternal influences on mammalian sex allocation. Trends in Ecology & Evolution, 29(3), 158–164.
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.
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.
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.
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.
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.
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.
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.
Grant, V. J. (2007). Could maternal testosterone levels govern mammalian sex ratio deviations? Journal of Theoretical Biology, 246(4), 708–719.
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.
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.
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.
Hedges, L. V., & Olkin, I. (2014). Statistical methods for meta-analysis. New York: Academic press.
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.
Higgins, J. P., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557–560.
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.
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.
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.
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.
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.
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.
Krackow, S. (1995). Potential mechanisms for sex ratio adjustment in mammals and birds. Biological Reviews, 70(2), 225–241.
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.
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.
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.
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.
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.
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.
Navara, K. J. (2013a). Hormone-mediated adjustment of sex ratio in vertebrates. Integrative and Comparative Biology, 53(6), 877–887.
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.
Pandian, T. J., & Sheela, S. G. (1995). Hormonal induction of sex reversal in fish. Aquaculture, 138(1), 1–22.
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.
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.
Pike, T. W., & Petrie, M. (2005). Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Animal Behaviour, 70(4), 745–751.
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.
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.
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.
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.
R Core Team. (2015). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.
Robert, K. A., & Schwanz, L. E. (2011). Emerging sex allocation research in mammals: Marsupials and the pouch advantage. Mammal Review, 41(1), 1–22.
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.
Rutkowska, J., & Cichoń, M. (2006). Maternal testosterone affects the primary sex ratio and offspring survival in zebra finches. Animal Behaviour, 71(6), 1283–1288.
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.
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.
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.
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.
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.
Viechtbauer, W. (2010). Conducting meta-analyses in R with the metafor package. Journal of Statistical Software, 36(3), 1–48.
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.
West, S. A. (2009). Sex allocation. Princeton, NJ: Princeton University Press.
West, S. A., & Sheldon, B. C. (2002). Constraints in the evolution of sex ratio adjustment. Science, 295(5560), 1685–1688.
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).
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Merkling, T., Nakagawa, S., Lagisz, M. et al. Maternal Testosterone and Offspring Sex-Ratio in Birds and Mammals: A Meta-Analysis. Evol Biol 45, 96–104 (2018). https://doi.org/10.1007/s11692-017-9432-9
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DOI: https://doi.org/10.1007/s11692-017-9432-9