Experimental evidence for homeostatic sex allocation after sex-biased reintroductions


First principles predict negative frequency-dependent sex allocation, but it is unproven in field studies and seldom considered, despite far-reaching consequences for theory and practice in population genetics and dynamics as well as animal ecology and behaviour. Twenty-four years of rhinoceros calving after 45 reintroductions across southern Africa provide the first in situ experimental evidence that unbalanced operational sex ratios predicted offspring sex and offspring sex ratios. Our understanding of population dynamics, especially reintroduction and invasion biology, will be significantly impacted by these findings.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: Sex allocation pattern and effect size.


  1. 1

    Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, 1930).

    Google Scholar 

  2. 2

    Werren, J. H. & Charnov, E. L. Nature 272, 349–350 (1978).

    CAS  Article  Google Scholar 

  3. 3

    Taylor, P. D. & Sauer, A. Am. Nat. 116, 305–310 (1980).

    Article  Google Scholar 

  4. 4

    Hamilton, W. D. Science 156, 477–488 (1967).

    CAS  Article  Google Scholar 

  5. 5

    Miller, T. E. X., Shaw, A. K., Inouye, B. D. & Neubert, M. G. Am. Nat. 177, 549–561 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  6. 6

    Lee, A. M., Saether, B. E. & Engen, S. Am. Nat. 177, 301–313 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7

    West, S. Sex Allocation (Princeton Univ. Press, 2009).

    Google Scholar 

  8. 8

    Owen-Smith, R. N. Megaherbivores: The Influence of Large Body Size on Ecology (Cambridge Univ. Press, 1988).

    Google Scholar 

  9. 9

    Williams, G. C. Proc. R. Soc. B-Biol. Sci. 205, 567–580 (1979).

    CAS  Article  Google Scholar 

  10. 10

    Linklater, W. et al. PLoS ONE 7, e30664 (2012).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11

    Linklater, W., MacDonald, E., Flamand, J. & Czekala, N. Animal Conserv. 13, 104–111 (2010).

    Article  Google Scholar 

  12. 12

    Lopez, S. & Dominguez, C. A. J. Evol. Biol. 16, 1177–1185 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13

    Olsson, M. & Shine, R. J. Evol. Biol. 14, 120–128 (2001).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14

    Linklater, W. Reprod. Fertil. Dev. 19, 831–839 (2007).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Caswell, H. & Weeks, D. E. Am. Nat. 128, 707–735 (1986).

    Article  Google Scholar 

  16. 16

    Lindstrom, J. & Kokko, H. Proc. R. Soc. B-Biol. Sci. 265, 483–488 (1998).

    CAS  Article  Google Scholar 

  17. 17

    Ranta, E., Lummaa, V., Kaitala, V. & Merila, J. Ecol. Lett. 3, 30–34 (2000).

    Article  Google Scholar 

  18. 18

    Gutowsky, L. F. G. & Fox, M. G. Hydrobiologia 671, 27–37 (2011).

    Article  Google Scholar 

  19. 19

    Hornett, E. A., Charlat, S., Wedell, N., Jiggins, C. D. & Hurst, G. D. D. Curr. Biol. 19, 1628–1631 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20

    Nakagawa, S. & Schielzeth, H. Biol. Rev. Cambridge Phil. Soc. 85, 935–956 (2010).

    Google Scholar 

Download references


This work was supported by granted funds from the US Fish & Wildlife Service administered Rhinoceros and Tiger Conservation Act of 1994 (grant agreement numbers 98210-2-G363, 98210-4-G920 and 98210-6-G102), International Rhino Foundation, Victoria University of Wellington, and Nelson Mandela Metropolitan University. Our thanks to K. Adcock, G. Kerley and M. Knight.

Author information




W.L.L. conceived the project; P.d.P. administered the programs that gathered the raw data from Namibian populations; W.L.L. and J.V.G. collated and conducted quality assurance of data; W.L.L., P.R.L. and J.V.G. conducted and interpreted analyses; W.L.L. wrote the first draft of the manuscript and all authors contributed to revisions.

Corresponding author

Correspondence to Wayne Leslie Linklater.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2 (PDF 228 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Linklater, W., Law, P., Gedir, J. et al. Experimental evidence for homeostatic sex allocation after sex-biased reintroductions. Nat Ecol Evol 1, 0088 (2017). https://doi.org/10.1038/s41559-017-0088

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing