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Female-biased sex ratios are associated with higher maternal testosterone levels in nutria (Myocastor coypus)

  • R. Fishman
  • Y. Vortman
  • U. Shanas
  • L. Koren
Original Article

Abstract

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.

Significance statement

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.

Keywords

Hair testing Invasive species Maternal testosterone Sex ratio Trivers–Willard 

Notes

Acknowledgments

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.

Ethical approval

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.

Supplementary material

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ESM 1 (XLSX 51 kb)
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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.The Mina and Everard Goodman Faculty of Life SciencesBar-Ilan UniversityRamat GanIsrael
  2. 2.Hula Research Center, Department of Animal SciencesTel-Hai CollegeUpper GalileeIsrael
  3. 3.Faculty of Life SciencesUniversity of Haifa-OranimTivonIsrael

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