Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression

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Abstract

In some species, females choose mates possessing ornaments that predict offspring survival1,2,3,4,5. However, sexual selection by female preference for male genetic quality6,7,8 remains controversial because conventional genetic mechanisms maintain insufficient variation in male quality to account for costly preference and ornament evolution9,10. Here we show that females prefer ornaments that indicate genetic quality generated by transmission conflict between the sex chromosomes. By comparing sex-ratio distributions in stalk-eyed fly (Cyrtodiopsis) progeny we found that female-biased sex ratios occur in species exhibiting eye-stalk sexual dimorphism11,12 and female preferences for long eye span13,14. Female-biased sex ratios result from meiotic drive15, the preferential transmission of a ‘selfish’ X-chromosome. Artificial selection for 22 generations on male eye-stalk length in sexually dimorphic C. dalmanni produced longer eye-stalks and male-biased progeny sex ratios in replicate lines. Because male-biased progeny sex ratios occur when a drive-resistant Y chromosome pairs with a driving X chromosome15, long eye span is genetically linked to meiotic drive suppression. Male eye span therefore signals genetic quality by influencing the reproductive value of offspring16.

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Figure 1: Sex-ratio distribution of male stalk-eyed flies, individuals were of the species: a, Cyrtodiopsis whitei; b, C. dalmanni; c, C. quinquegutta.
Figure 2: Replicate bidirectional response to selection on male eye-span to body-length ratio plotted against generation for eye span expressed as differences from control line averages.
Figure 3: Sex-ratio distributions of male Cdalmanni after 22 generations of selection.
Figure 4: Correlation between mean male eye span and chromosome frequency.

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Acknowledgements

We thank H. S. Yong, P. Reillo and M. Taper for assistance in the field; S. Bhatt, P.Reillo and D. Reames for assistance in the laboratory; and C. Boake, R. Gibson, L. Hurst, M. Kirkpatrick, R. Trivers and L. Wolfenbarger for comments on the manuscript. This work was supported by the NSF.

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Correspondence to Gerald S. Wilkinson.

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