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Sexual selection protects against extinction

Nature volume 522, pages 470–473 (2015)Cite this article

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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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Figure 1: Extinction trajectories under increasing inbreeding differ between family lines derived from strong (red squares) versus weak (blue circles) sexual selection histories.
Figure 2: Reproductive fitness declines under increasing inbreeding of families derived from strong (red squares) versus weak (blue circles) sexual selection histories differ in magnitude and rate.

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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

  1. Alyson J. Lumley and Łukasz Michalczyk: These authors contributed equally to this work.

Authors and 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, Kraków, 30-387, Poland

    Łukasz Michalczyk

  3. ETH Zurich, Institute of Integrative Biology, D-USYS, Universitatsstrasse 16, CHN J 11, Zürich, 8092, 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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  1. Alyson J. Lumley
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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.

Corresponding author

Correspondence to Matthew J. G. Gage.

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Competing interests

The authors declare no competing financial interests.

Additional information

Data sets for all experiments and assays have been deposited in the Dryad Digital Repository at http://dx.doi.org/10.5061/dryad.86750.

Extended data figures and tables

Extended Data Figure 1 Experimental rationale for purging and then exposing mutation load.

Having been changed by strong (+SS, red) versus weak (−SS, blue) histories of sexual selection, while under equal influences of natural selection (NS), variation in mutation load residing in the form of recessive alleles is exposed via inbreeding. Inbreeding was enforced through monogamous sib × sib pairings, also eliminating concurrent confounds of interlocus sexual conflict. Populations with reduced mutation load as a result of histories of strong sexual selection are predicted to resist extinction (survival, s) and maintain fitness (f) under continuous inbreeding (i).

Extended Data Figure 2 Experimental evolution protocols for regimes A and B.

Contrasting intensities of strong (red) versus weak (blue) sexual selection were imposed upon each generation of adult reproduction, while equalizing effective population size within a regime, and allowing full genetic mixing within the replicate lines at the egg/larval/pupal stages. From the start, each treatment was replicated to create three independent lines. Regime A (a) applied contrasting sexual selection by varying adult operational sex ratio, while regime B (b) enforced monogamy to compare against polyandry.

Extended Data Figure 3 Extinction and fitness decline protocols.

Inbreeding in family lines was performed via sib × sib crosses for up to 20 generations across 3 years. To measure extinction (a), a family was considered extinct when it failed to produce offspring, or offspring were of the same sex (which occurred in only 9 out of 216 family lines, indicating no sex-specific pre-adult mortality by treatment). In regime A, extinction data were collected from 28 initial families per line, three lines per sexual selection treatment, comparing both strong versus weak treatments (n = 168 total family lines). In regime B, extinction data were collected from eight initial families per line, three lines per sexual selection treatment, comparing both strong versus weak treatments (n = 48 total family lines). To measure fitness decline (b), two additional sib × sib pairs per family per generation were bred to estimate reproductive fitness in every generation by counting number of offspring produced (see Methods). In both regimes A and B, fitness data were collected from eight initial families per line, three lines per sexual selection treatment, and both strong versus weak treatment contrasts in each.

Extended Data Figure 4 Estimated heterozygosity (±s.e.m.) does not differ between experimental evolution sexual selection treatments within regime A (left) and regime B (right).

Linear mixed effect modelling showed the estimated heterozygosity of the male-biased selection treatment (M: Hest = 0.312, t = 9.468) is not significantly different from that of female-biased (F: Hest = 0.318, t = 9.295, P = 0.863), but is significantly different from monogamous and polyandrous treatments (Mo: Hest = 0.199, t = 6.453, P = 0.003; Po: Hest = 0.197, t = 6.397, P = 0.003). The estimated heterozygosities of monogamous and polyandrous treatments are not significantly different (P = 0.956) (see Methods).

Source data

Extended Data Figure 5 Concordance between raw data and model fit in extinction analyses.

Survival curves of raw data (thick and dotted lines) overlaid on model fit (shaded areas with mean curves and 95% confidence intervals). Survival of families derived from strong (red, solid line) or weak (blue, dotted line) sexual selection treatment histories differed: (a) regime A, male-biased (red) versus female-biased (blue) sexual selection treatments; (b) regime B, polyandrous (red) versus monogamous (blue); (c) regimes A and B combined into a single analysis. See Fig. 1 and the main text for results of statistical analyses, and Methods and Extended Data Figs 2 and 3 for details of protocols, methods and experimental design.

Source data

Extended Data Figure 6 Regime A.

Boxplots of the relationships between fitness and inbreeding generation for the male-biased (a and c) versus the female-biased (b and d) treatments. Curves show the predicted relationships between reproductive fitness and inbreeding generation from the GLMMs, and the narrow red and blue shadows show the 95% confidence intervals predicted from the fixed effects. Horizontal bars indicate medians, boxes indicate interquartile ranges, whiskers indicate minimum and maximum values, and circles indicate outliers (values 1.5 times higher or lower than the first and third quartiles, respectively). Comparison of a versus b identifies the difference in total fitness declines between strong versus weak sexual selection histories in regime A, while c versus d identifies the same difference in decline for fitness but only for the sibling pairs that produced at least some offspring (that is, omitting zero fitness values that may have resulted from a failure to mate). See Fig. 1, main text and Extended Data Table 1 for results of statistical analyses.

Source data

Extended Data Figure 7 Regime B.

Boxplots of the relationships between fitness and inbreeding generation for the polyandrous (a and c) versus the monogamous (b and d) treatments. Curves show the predicted relationships between reproductive fitness and inbreeding generation from the GLMMs, and the narrow red and blue shadows show the 95% confidence intervals predicted from the fixed effects. Horizontal bars indicate medians, boxes indicate interquartile ranges, whiskers indicate minimum and maximum values, and circles indicate outliers (values 1.5 times higher or lower than first and third quartiles, respectively). Comparison of a versus b identifies the difference in total fitness declines between strong versus weak sexual selection histories in regime B, while c versus d identifies the same difference in decline for fitness but only for the sibling pairs that produced at least some offspring (that is, omitting zero fitness values that may have resulted from a failure to mate). See Fig. 1, main text and Extended Data Table 1 for results of statistical analyses.

Source data

Extended Data Figure 8 Across 7 days of mating opportunity, males successfully inseminated 50 females on average (±s.e.m.).

Six virgin females were allocated to individual GA1 control stock males (n = 11) every 12 h for 7 days, providing males with 84 potential mates. Over this 1 week period (replicating that applied within the experimental evolution protocols, Extended Data Fig. 2), males successfully inseminated and generated offspring from an average of 50 females (see Methods).

Source data

Extended Data Table 1 Fixed-effect parameter estimates from negative binomial GLMMs of the relationship between fitness and generation of inbreeding for male-biased and female-biased treatments (regime A), and polyandrous and monogamous treatments (regime B), and their statistical interactions. See Methods for details of replication and sample sizes.
Full size table

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, Supplementary Tables 1-2 and additional references. (PDF 1015 kb)

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). (ZIP 5 kb)

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Lumley, A., Michalczyk, Ł., Kitson, J. et al. Sexual selection protects against extinction. Nature 522, 470–473 (2015). https://doi.org/10.1038/nature14419

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