Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females

Abstract

Females commonly mate with more than one male1, and polyandry has been shown to increase reproductive success in many species2,3,4. Insemination by multiple males shifts the arena for sexual selection from the external environment to the female reproductive tract, where sperm competition or female choice of sperm could bias fertilization against sperm from genetically inferior5 or genetically incompatible males6,7. Evidence that polyandry can be a strategy for avoiding incompatibility comes from studies showing that inbreeding cost is reduced in some egg-laying species by postcopulatory mechanisms that favour fertilization by sperm from unrelated males8,9,10. In viviparous (live-bearing) species, inbreeding not only reduces offspring genetic quality but might also disrupt feto-maternal interactions that are crucial for normal embryonic development11,12,13. Here we show that polyandry in viviparous pseudoscorpions reduces inbreeding cost not through paternity-biasing mechanisms favouring outbred offspring, but rather because outbred embryos exert a rescuing effect on inbred half-siblings in mixed-paternity broods. The benefits of polyandry may thus be more complex for live-bearing females than for females that lay eggs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Effect of mating treatment on brood production.
Figure 2: Number of nymphs born versus proportion outbred in successful NS and SN broods.

Similar content being viewed by others

References

  1. Jennions, M. D. & Petrie, M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. Camb. Phil. Soc. 75, 21–64 (2000)

    Article  CAS  Google Scholar 

  2. Hasselquist, D., Bensch, S. & von Schantz, T. Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229–232 (1996)

    Article  CAS  ADS  Google Scholar 

  3. Tregenza, T. & Wedell, N. Polyandrous females avoid the costs of inbreeding. Nature 415, 71–73 (2002)

    Article  CAS  ADS  Google Scholar 

  4. Stockley, P. Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc. R. Soc. Lond. B 270, 271–278 (2003)

    Article  CAS  Google Scholar 

  5. Birkhead, T. R., Møller, A. P. & Sutherland, W. J. Why do females make it so difficult for males to fertilize their eggs? J. Theor. Biol. 161, 51–60 (1993)

    Article  Google Scholar 

  6. Zeh, J. A. & Zeh, D. W. Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61, 1051–1063 (2001)

    Article  Google Scholar 

  7. Tregenza, T. & Wedell, N. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013–1027 (2000)

    Article  CAS  Google Scholar 

  8. Olsson, M., Shine, R., Madsen, T., Gullberg, A. & Tegelström, H. Sperm selection by females. Nature 383, 585 (1996)

    Article  CAS  ADS  Google Scholar 

  9. Foerster, K., Delhey, K., Johnsen, A., Lifjeld, J. T. & Kempenaers, B. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425, 714–717 (2003)

    Article  CAS  ADS  Google Scholar 

  10. Bretman, A., Wedell, N. & Tregenza, T. Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc. R. Soc. Lond. B 271, 159–164 (2004)

    Article  CAS  Google Scholar 

  11. Ober, C. et al. Variation in the HLA-G promoter region influences miscarriage rates. Am. J. Human Genet. 72, 1425–1435 (2003)

    Article  CAS  Google Scholar 

  12. Choudhury, S. R. & Knapp, L. A. Human reproductive failure II: immunogenetic and interacting factors. Human Reprod. Update 7, 135–160 (2001)

    Article  CAS  Google Scholar 

  13. Davies, C. J. et al. Major histocompatibility antigen expression on the bovine placenta: its relationship to abnormal pregnancies and retained placenta. Anim. Reprod. Sci. 82–83, 267–280 (2004)

    Article  Google Scholar 

  14. Keller, L. F. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241 (2002)

    Article  Google Scholar 

  15. Hill, J. A. in Immunology of Human Reproduction (eds Kurpisz, M. & Fernandez, N.) 401–424 (Bios Scientific, Oxford, UK, 1995)

    Google Scholar 

  16. Weygoldt, P. The Biology of Pseudoscorpions (Harvard Univ. Press, Cambridge, MA, 1969)

    Google Scholar 

  17. Newcomer, S. D., Zeh, J. A. & Zeh, D. W. Genetic benefits enhance the reproductive success of polyandrous females. Proc. Natl Acad. Sci. USA 96, 10236–10241 (1999)

    Article  CAS  ADS  Google Scholar 

  18. Zeh, D. W., Zeh, J. A. & Bermingham, E. Polyandrous, sperm-storing females: carriers of male genotypes through episodes of adverse selection. Proc. R. Soc. Lond. B 264, 119–125 (1997)

    Article  ADS  Google Scholar 

  19. Zeh, D. W., Zeh, J. A. & May, C. A. Charomid cloning vectors meet the pedipalpal chelae: single-locus minisatellite DNA probes for paternity assignment in the harlequin beetle-riding pseudoscorpion. Mol. Ecol. 3, 517–522 (1994)

    Article  CAS  Google Scholar 

  20. Rosenthal, R. & Rosnow, R. L. Contrast Analysis. Focused Comparisons in the Analysis of Variance (Cambridge Univ. Press, Cambridge, UK, 1985)

    Google Scholar 

  21. Simmons, L. W. The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J. Evol. Biol. 14, 585–594 (2001)

    Article  Google Scholar 

  22. Hoffmann, J. A. The immune response of Drosophila. Nature 426, 33–38 (2003)

    Article  CAS  ADS  Google Scholar 

  23. Caucheteux, S. M., Kanellopoulos-Langevin, C. & Ojcius, D. M. At the innate frontiers between mother and fetus: linking abortion with complement activation. Immunity 18, 169–172 (2003)

    Article  CAS  Google Scholar 

  24. Haig, D. Genetic conflicts in human pregnancy. Q. Rev. Biol. 68, 495–532 (1993)

    Article  CAS  Google Scholar 

  25. Jennions, M. D., Hunt, J., Graham, R. & Brooks, R. No evidence for inbreeding avoidance through postcopulatory mechanisms in the black field cricket, Teleogryllus commodus. Evolution 58, 2472–2477 (2004)

    Article  Google Scholar 

  26. SAS Institute, The SAS System for Windows, Release 8.02 (SAS Institute, Cary, 2001)

    Google Scholar 

  27. Schluter, D. & Nychka, D. Exploring fitness surfaces. Am. Nat. 143, 597–616 (1994)

    Article  Google Scholar 

Download references

Acknowledgements

We thank M. Bonilla and S. Trimmer for assistance; K. Panter for discussion; the Smithsonian Tropical Research Institute for logistical support; and La Autoridad Nacional del Ambiente for permission to collect in Panama. This research was supported by grants from the US National Science Foundation and the National Geographic Society. Author Contributions J.A.Z. designed the study, carried out the mating and rearing experiments, and took the primary role in writing the paper. D.W.Z. performed the molecular and statistical analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeanne A. Zeh.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Methods

This file contains the full, detailed version of the Methods. (DOC 46 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zeh, J., Zeh, D. Outbred embryos rescue inbred half-siblings in mixed-paternity broods of live-bearing females. Nature 439, 201–203 (2006). https://doi.org/10.1038/nature04260

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04260

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

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