This article has been updated


Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring1. It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load2,3,4. Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through ‘genic capture’5 could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Change history

  • 24 June 2015

    Minor changes were made to author affiliation number 4.


  1. 1.

    The Evolution of Sex (Cambridge Univ. Press, 1978)

  2. 2.

    Sexual selection and the maintenance of sexual reproduction. Nature 411, 692–695 (2001)

  3. 3.

    Sexual selection and the maintenance of sex. Nature 411, 689–692 (2001)

  4. 4.

    & Purging the genome with sexual selection: reducing mutation load through selection on males. Evolution 63, 569–582 (2009)

  5. 5.

    , , & Genic capture and resolving the lek paradox. Trends Ecol. Evol. 19, 323–328 (2004)

  6. 6.

    Sexual Selection (Princeton Univ. Press, 1994)

  7. 7.

    & Mutation load: the fitness of individuals in populations where deleterious alleles are abundant. Annu. Rev. Ecol. Syst. 43, 115–135 (2012)

  8. 8.

    & The consequences of polyandry for population viability, extinction risk and conservation. Phil. Trans. R. Soc. B 368, (2013)

  9. 9.

    Mutation, mean fitness, and genetic load. Oxf. Surv. Evol. Biol. 9, 3–42 (1993)

  10. 10.

    & Toward a realistic model of mutations affecting fitness. Evolution 57, 683–685 (2003)

  11. 11.

    The effect of variation of fitness. Am. Nat. 71, 337–349 (1937)

  12. 12.

    et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56–65 (2012)

  13. 13.

    On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life (John Murray, 1859)

  14. 14.

    & Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution 58, 1028–1037 (2004)

  15. 15.

    et al. Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum. Evolution 65, 713–724 (2011)

  16. 16.

    Effectiveness of sexual selection in removing mutations induced with ionizing radiation. Ecol. Lett. 7, 1149–1154 (2004)

  17. 17.

    , & Sexual selection accelerates the elimination of a deleterious mutant in Drosophila melanogaster. Evolution 63, 324–333 (2009)

  18. 18.

    & Sexual selection can remove an experimentally induced mutation load. Evolution 68, 295–300 (2014)

  19. 19.

    & Mating density and the strength of sexual selection against deleterious alleles in Drosphila melanogaster. Evolution 62, 857–867 (2008)

  20. 20.

    & Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster. Evolution 66, 2127–2137 (2012)

  21. 21.

    & Populations with elevated mutation load do not benefit from the operation of sexual selection. J. Evol. Biol. 24, 1918–1926 (2011)

  22. 22.

    & Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA 96, 5083–5088 (1999)

  23. 23.

    & The genetic basis of inbreeding depression. Genet. Res. 74, 329–340 (1999)

  24. 24.

    Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984)

  25. 25.

    et al. BeetleBase in 2010: revisions to provide comprehensive genomic information for Tribolium castaneum. Nucleic Acids Res. 38, D437–D442 (2010)

  26. 26.

    , , , & Evolution under monogamy feminizes gene expression in Drosophila melanogaster. Nature Commun. 5, (2014)

  27. 27.

    , & The effect of sexual selection on offspring fitness depends on the nature of genetic variation. Curr. Biol. 22, 204–208 (2012)

  28. 28.

    et al. Inbreeding promotes female promiscuity. Science 333, 1739–1742 (2011)

  29. 29.

    Genetics and demography in biological conservation. Science 241, 1455–1460 (1988)

  30. 30.

    & in Conservation Biology: The Science of Scarcity and Diversity (ed. Soulé, M. E.) 19–34 (Sinauer Associates, 1986)

  31. 31.

    et al. Experimental removal of sexual selection reveals adaptations to polyandry in both sexes. Evol. Biol. 41, 62–70 (2014)

  32. 32.

    & Introduction to Quantitative Genetics 4th edn (Pearson Education, 1996)

  33. 33.

    A package for survival analysis in S. R package version 2.37-7. (2014)

  34. 34.

    R Core Team. R: a language and environment for statistical computing (R Foundation for Statistical Computing, 2013)

  35. 35.

    et al. AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimiz. Meth. Software 27, 233–249 (2012)

  36. 36.

    & Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010)

  37. 37.

    , , & lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-6. (2014)

  38. 38.

    , & lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-6. (2014)

Download references


We thank the Natural Environment Research Council and the Leverhulme Trust for financial support, D. Edward for statistical advice and colleagues at the 2013 Biology of Sperm meeting for comments that improved analytical design and interpretation.

Author information

Author notes

    • Alyson J. Lumley
    •  & Łukasz Michalczyk

    These authors contributed equally to this work.


  1. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK

    • Alyson J. Lumley
    • , James J. N. Kitson
    • , Lewis G. Spurgin
    • , Catriona A. Morrison
    • , Joanne L. Godwin
    • , Matthew E. Dickinson
    • , Tracey Chapman
    •  & Matthew J. G. Gage
  2. Department of Entomology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland

    • Łukasz Michalczyk
  3. ETH Zurich, Institute of Integrative Biology, D-USYS, Universitatsstrasse 16, CHN J 11, 8092 Zürich, Switzerland

    • Oliver Y. Martin
  4. Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), C/Astrofísico Francisco Sánchez 3, 38206 San Cristóbal de La Laguna, Santa Cruz de Tenerife, Canary Islands, Spain

    • Brent C. Emerson


  1. Search for Alyson J. Lumley in:

  2. Search for Łukasz Michalczyk in:

  3. Search for James J. N. Kitson in:

  4. Search for Lewis G. Spurgin in:

  5. Search for Catriona A. Morrison in:

  6. Search for Joanne L. Godwin in:

  7. Search for Matthew E. Dickinson in:

  8. Search for Oliver Y. Martin in:

  9. Search for Brent C. Emerson in:

  10. Search for Tracey Chapman in:

  11. Search for Matthew J. G. Gage in:


Ł.M., O.Y.M. and M.J.G.G. initiated the experimental evolution lines used in this work in 2005 and, with A.J.L., have maintained them since. M.J.G.G., Ł.M. and A.J.L. conceived, designed, conducted and analysed the study, with input from B.C.E. and T.C. J.J.N.K. and L.G.S. ran the microsatellite analyses. J.L.G., M.E.D. and O.Y.M. helped with line maintenance and experimental data collection. C.A.M. performed the fitness analyses. M.J.G.G. and A.J.L. wrote the paper, with contributions from all authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Matthew J. G. Gage.

Data sets for all experiments and assays have been deposited in the Dryad Digital Repository at

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text and Data, Supplementary Tables 1-2 and additional references.

Zip files

  1. 1.

    Supplementary Data

    This zipped file contains the following: Figure 1 R analysis script (Extinction Script.R); Figure 2 R analysis script (Fitness Script.R) and Extended data Figure 4 R analysis script (Heterozygosity Script.R).

About this article

Publication history





Further reading


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.