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Experimental evidence for effects of sexual selection on condition-dependent mutation rates

Abstract

Sexual selection depletes genetic variation but depleted genetic variation limits the efficacy of sexual selection—a long-standing enigma known as the lek paradox. Here we offer a twist to this paradox by showing that sexual selection and the generation of new genetic variation via mutation may be entangled in an evolutionary feedback loop. We induced DNA damage in the germline of male seed beetles evolved under regimes manipulating the opportunity for natural and sexual selection, and quantified de novo mutations in F2–F7 generations by measuring mutation load. Sexually selected males passed on smaller loads, suggesting that selection for male quality not only purges segregating deleterious alleles, but can also reduce the rate at which such alleles originate de novo. However, when engaging in socio-sexual interactions, males evolved exclusively under sexual selection transferred greater loads, suggesting that trade-offs between naturally and sexually selected fitness components can increase mutation rate. These results offer causality to the widely observed male mutation bias and have implications for the maintenance of genetic variation in fitness.

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Fig. 1: De novo dominant mutation load passed on to F2 offspring.
Fig. 2: De novo recessive mutation load passed on to offspring generations F3–F7 measured as lineage extinction during successive full-sibling mating.

Data availability

The data are available at https://doi.org/10.6084/m9.figshare.c.4838352.v1. Generated empirical data are presented in Figs. 1 and 2, Extended Data Figs. 1–5 and Supplementary Figs. 1–5.

Code availability

R code for MCMC models is available in the Supplementary information.

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Acknowledgements

The authors thank J. Liljestrand-Rönn, K. Gotthard and T. Sangsuwan for help in the laboratory and for providing access to the radiation source. This work has also benefitted greatly from discussions with members of the seed beetle research group and C. Rueffler at Uppsala University. This work was supported by a grant from the Swedish Research Council VR (no. 2015-05223) to D.B.

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D.B. conceived the research and general experimental design. J.B. developed details of the design, collected and analysed data and produced figures with input and assistance from D.B. D.B. and J.B. wrote the manuscript.

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Correspondence to David Berger.

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Extended data

Extended Data Fig. 1 Experimental design used to measure germline maintenance via de novo dominant mutation load.

Illustration of the experimental procedures used for the assessment of dominant mutation load. After 29 generations of experimental evolution, all lines were maintained for 1 generation in a common garden under a polygamous mating regime to counteract potential parental (non-genetic) effects from the mating regime. Freshly emerged virgin males (0–24h after eclosion) were either isolated in 0.3ml Eppendorf tubes (five isolated beetles in one Petri dish) or kept together in groups of five together with five standard females, allowed to interact and mate freely, for 23 hours. Within one hour after the socio-sexual treatment, beetles were exposed to 25Gy of gamma radiation (30 minutes of exposure). Subsequently, all beetles, including control individuals that only underwent the socio-sexual but not the irradiation treatment, were mated with a standard female once to remove putatively damaged ejaculate and to be challenged to regenerate a new ejaculate. After 25 hours, all beetles were mated once with a standard female. To exclude the possibility of putative parental effects caused by irradiation, dominant mutation load was estimated by counts of adult F2 offspring. To that end, F1 offspring of irradiated and control males were propagated using a Middleclass Neighbourhood crossing scheme, effectively relaxing selection on all but the unconditionally lethal dominant mutations. Inbreeding was avoided by making crosses among F1 families applying a round-robin mating design.

Extended Data Fig. 2 Experimental design used to measure germline maintenance via de novo recessive mutation load.

Illustration of the inbreeding protocol used to assess recessive de novo mutation load. To exclude the possibility that effects of genetic background and possible non-genetic parental effects affected results, recessive lethals were scored on backgrounds constructed by crosses between alternative combinations of socio-sexual treatments (isolated virgins or reproducing in groups) and selection regimes (N- or S-males), equalizing the mean contribution of each original background in the inbred lineages. We recorded lineage extinction rate over five generations after the onset of inbreeding as an estimate of recessive mutation load.

Extended Data Fig. 3 Mating behavior.

Mating, mounting and locomotor activity of the respective regimes (NS: yellow, N: red, S: blue) as a function of time over the three periods of observation. The first vertical dotted line indicates the separation between the initial high mating-frequency phase immediately after putting males and females into contact and the subsequent phase of behaviour. The second and third vertical dotted lines indicate the beginning of the second (2.5h after initiation) and third (daybreak of the following day) observation period.

Extended Data Fig. 4 Ejaculate production.

Line specific (light and dark lines within each regime) relative ejaculate weight for mating two and three for beetles kept in isolation for ejaculate regeneration (solid lines) or in social groups of five males (dashed lines) (means ± 95% confidence limits).

Extended Data Fig. 5 Sperm production.

In a) the number of sperm transferred at the third mating and at the fourth mating following a 25h recovery period during which males were kept isolated, for NS (yellow), N (red) and S (blue) males. Shown are means per replicate line. In b) the number of sperm transferred at the third mating and at the fourth mating following a recovery period of 7h during which males were kept isolated (solid lines) or in groups of three (dashed lines). In c) the difference between the number of transferred sperm in mating 4 and 3 for replicate evolution lines and social treatment. NS males transferred more sperm overall (a). S-males, evolved under only sexual selection, show a different response to social treatment than N- and NS-males that had evolved under natural selection (c).

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Baur, J., Berger, D. Experimental evidence for effects of sexual selection on condition-dependent mutation rates. Nat Ecol Evol 4, 737–744 (2020). https://doi.org/10.1038/s41559-020-1140-7

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