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Abstract

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.

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Change history

  • 24 June 2015

    Minor changes were made to author affiliation number 4.

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Acknowledgements

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.

Affiliations

  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

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Contributions

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 http://dx.doi.org/10.5061/dryad.86750.

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    Supplementary Information

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

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    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).

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DOI

https://doi.org/10.1038/nature14419

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