Female-biased sex ratios are associated with higher maternal testosterone levels in nutria (Myocastor coypus)
Under various ecological conditions, producing a biased sex ratio may be adaptive. However, the factors that translate specific ecological conditions into internal processes remain an enigma. A potential mediator is maternal testosterone, which may reflect physical, reproductive, and social conditions. The nutria (Myocastor coypus) is a polygynous rodent, invasive in many parts of the world, which shows fluctuating sex ratios. Using necropsies of 82 pregnant culled nutrias, we found that in early pregnancy, offspring sex ratios are more male-biased than in later pregnancy. Since sex ratios decrease with pregnancy age, male fetuses in our study population may be terminated. In 68% of the litters, the heaviest fetus was a male, suggesting that males are the “expensive” sex. We also found that while maternal weight was not associated with testosterone, heavier females and those with lower testosterone had male-biased sex ratios. Litters of high testosterone females had female-biased sex ratios. To the best of our knowledge, this study is the first to show a negative association between maternal testosterone and male-biased sex ratios. Testosterone, through its role in reproduction, might be mediating maternal internal and external conditions by adjusting intra-uterine sex ratio.
For decades, the mechanisms behind offspring sex ratios have been of interest across disciplines. Maternal testosterone has been implicated in mediating maternal condition, thus influencing secondary sex ratios. Here, we investigated the reproductive parameters of a culled nutria and integrated it with maternal hair testosterone levels to test the association between long-term testosterone and sex ratios. Our most surprising result was that high maternal testosterone levels were related with female-biased sex ratios. This is contrary to previous studies in other species and counter-intuitive. Heavier females tended to have male-biased litters. We also found that the proportionate representation of males within litters declined over the course of pregnancy. Male fetuses were usually the heaviest fetus, suggesting that they are the more “expensive” sex. We believe that our study provides new insights in this long-debated issue and will contribute to understanding the reproductive costs involved with maternal testosterone across animal models.
KeywordsHair testing Invasive species Maternal testosterone Sex ratio Trivers–Willard
We are grateful to Dr. Devorah Matas for developing the method for molecular sexing of fetuses in the Koren Lab, as well as her devoted support. We thank Itai Dolev, Sharon Dolev, and Liran Tal for collecting nutrias and their all heartedly support, and the Jewish National Fund (KKL-JNF) for permission to work in the Agamon Hula Park. We also thank our many undergraduate student assistants, particularly Ari Timokhin, Elina Tsirulnikov, Nataly Navon, and Dor Nehoray, and our field assistant Linor Aviram. We are obliged to Prof. Eli Geffen, Prof. James Hare, and an anonymous reviewer for their constructive comments and to Sharon Victor for English editing.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
The nutria was introduced into the wild in Israel during the 1950s and is currently considered a pest. Culling efforts are managed by the KKL-JNF, the managing organization of the Agmon Hula Park. We collected nutria that were culled during 2013–2015 and did not initiate culling. No permits are needed for collecting nutrias since they are not protected by the Israeli law.
- Arnon L, Hazut N, Tabachnik T, Weller A, Koren L (2016) Maternal testosterone and reproductive outcome in a rat model of obesity. Theriogenology 86:1042–1047. https://doi.org/10.1016/j.theriogenology.2016.03.033 PubMedCrossRefGoogle Scholar
- Correa SM, Horan CM, Johnson PA, Adkins-Regan E (2011) Copulatory behaviors and body condition predict post-mating female hormone concentrations, fertilization success, and primary sex ratios in Japanese quail. Horm Behav 59:556–564. https://doi.org/10.1016/j.yhbeh.2011.02.009 PubMedCrossRefGoogle Scholar
- Diez C, Bermejo-Alvarez P, Trigal B, Caamaño JN, Muñoz M, Molina I, Gutiérrez-Adán A, Carrocera S, Martín D, Gómez E (2009) Changes in testosterone or temperature during the in vitro oocyte culture do not alter the sex ratio of bovine embryos. J Exp Zool Part A 311:448–452. https://doi.org/10.1002/jez.540 CrossRefGoogle Scholar
- Gosling LM (1983) The adaptive control of offspring sex ratio by female coypus (Myocastor coypus). Am Zool 23:934–934Google Scholar
- Gosling LM, Baker SJ (1989) Demographic consequences of differences in the ranging behaviour of male and female coypus. In: Putman RJ (ed) Mammals as pests. Chapman and Hall, London, pp 155–167Google Scholar
- Gosling LM, Baker SJ, Wright KMH (1984) Differential investment by female coypus (Myocastor coypus) during lactation. Symp Zool Soc Lond 51:273–300Google Scholar
- Hotchkiss AK, Vandenbergh JG (2005) The anogenital distance index of mice (Mus musculus domesticus): an analysis. J Am Assoc Lab Anim 44:46–48Google Scholar
- Lara HE, Dorfman M, Venegas SM, Luza SL, Luna A, Mayerhofer MA, Guimaraes RES, Ramirez VD (2002) Changes in sympathetic nerve activity of the mammalian ovary during a normal estrous cycle and in polycystic ovary syndrome: studies on norepinephrine release. Microsc Res Tech 59:495–502. https://doi.org/10.1002/jemt.10229 PubMedCrossRefGoogle Scholar
- Leblanc DJ (1994) Nutria. In: Hygnstrom SE, Timm RM, Larson GE (eds) The handbook: prevention and control of wildlife damage. University of Nebraska Cooperative Extension, Lincoln, USA, pp 71–80Google Scholar
- Liening SH, Stanton SJ, Saini EK, Schultheiss OC (2010) Salivary testosterone, cortisol, and progesterone: two-week stability, interhormone correlations, and effects of time of day, menstrual cycle, and oral contraceptive use on steroid hormone levels. Physiol Behav 99:8–16. https://doi.org/10.1016/j.physbeh.2009.10.001 PubMedCrossRefGoogle Scholar
- Moore FR, Al Dujaili EAS, Cornwell RE, Smith ML, Lawson JF, Sharp M, Perrett DI (2011) Cues to sex- and stress-hormones in the human male face: functions of glucocorticoids in the immunocompetence handicap hypothesis. Horm Behav 60:269–274. https://doi.org/10.1016/j.yhbeh.2011.05.010 PubMedCrossRefGoogle Scholar
- Nabozny M, Natanek A, Piorkowska M (2015) The influence of age on histological parameters of Greenland nutria hair coat. Rocz Nauk Zootech 42:55–67Google Scholar
- Nathanielsz PW, Rossdale PD, Silver M, Comline RS (1975) Studies on fetal, neonatal and maternal cortisol metabolism in the mare. J Reprod Fertil 23:625–630Google Scholar
- Newson RM (1966) Reproduction in the feral coypu (Myocastor coypus). Symp Zool Soc Lond 15:323–334Google Scholar
- Ryan CP, Anderson WG, Berkvens CN, Hare JF (2014) Maternal gestational cortisol and testosterone are associated with trade-offs in offspring sex and number in a free-living rodent (Urocitellus richardsonii). PLoS One 9:e111052. https://doi.org/10.1371/journal.pone.0111052 PubMedPubMedCentralCrossRefGoogle Scholar
- Shargal D, Shore L, Roteri N, Terkel A, Zorovsky Y, Shemesh M, 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 69:673–680. https://doi.org/10.1016/j.theriogenology.2007.11.017 PubMedCrossRefGoogle Scholar
- Willner GR, Chapman JA, Pursley D (1979) Reproduction, physiological-responses, food-habits, and abundance of nutria on Maryland marshes. Wildlife Monogr 65:1–43Google Scholar
- Wilson AS, Brown EL, Villa C, Lynnerup N, Healey A, Ceruti MC, Reinhard J, Previgliano CH, Araoz FA, Gonzalez Diez J, Taylor T (2013) Archaeological, radiological, and biological evidence offer insight into Inca child sacrifice. P Natl Acad Sci USA 110:13322–13327. https://doi.org/10.1073/pnas.1305117110 CrossRefGoogle Scholar