A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success

Abstract

Male reproductive success depends on the competitive ability of sperm to fertilize the ova, which should lead to strong selection on sperm characteristics. This raises the question of how heritable variation in sperm traits is maintained. Here we show that in zebra finches (Taeniopygia guttata) nearly half of the variance in sperm morphology is explained by an inversion on the Z chromosome with a 40% allele frequency in the wild. The sperm of males that are heterozygous for the inversion had the longest midpieces and the highest velocity. Furthermore, such males achieved the highest fertility and the highest siring success, both within-pair and extra-pair. Males homozygous for the derived allele show detrimental sperm characteristics and the lowest siring success. Our results suggest heterozygote advantage as the mechanism that maintains the inversion polymorphism and hence variance in sperm design and in fitness.

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Figure 1: Sperm morphology as a function of male Z-chromosome inversion type.
Figure 2: Sperm swimming speed as a function of male Z-chromosome inversion type.
Figure 3: Male siring success as a function of male Z-chromosome inversion type.

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Acknowledgements

We thank T. Aronson, E. Bolund, S. Janker, H. Schielzeth, J. Schreiber and O. Tomášek for help with data collection, M. Schneider and G. Hemmrich-Stanisak for molecular and genomic work, and S. Bauer, E. Bodendorfer, J. Didsbury, A. Grötsch, A. Kortner, P. Neubauer, F. Weigel and B. Wörle for animal care and help with breeding. This work was supported by the Max Planck Society (B.K.) and by the Czech Science Foundation (project no. P506/12/2472 to T.A.).

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U.K., M.W. and A.F. genotyped all birds. T.A., J.A. and K.M. collected sperm samples. P.O. measured sperm morphology. J.A. measured sperm velocity. W.F., M.I., D.W. and K.M. collected breeding data. U.K., W.F. and Y.P. analysed the data. U.K., W.F. and B.K. wrote the manuscript with help from T.A. All authors contributed to the final manuscript. W.F., T.A. and B.K. conceived of the study.

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Correspondence to Wolfgang Forstmeier.

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Knief, U., Forstmeier, W., Pei, Y. et al. A sex-chromosome inversion causes strong overdominance for sperm traits that affect siring success. Nat Ecol Evol 1, 1177–1184 (2017). https://doi.org/10.1038/s41559-017-0236-1

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