Article

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

  • Nature Ecology & Evolution 111771184 (2017)
  • doi:10.1038/s41559-017-0236-1
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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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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.).

Author information

Affiliations

  1. Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Seewiesen, 82319, Germany

    • Ulrich Knief
    • , Wolfgang Forstmeier
    • , Yifan Pei
    • , Malika Ihle
    • , Daiping Wang
    • , Katrin Martin
    •  & Bart Kempenaers
  2. Division of Evolutionary Biology, Faculty of Biology, Ludwig Maximilian University of Munich, Planegg-Martinsried, 82152, Germany

    • Ulrich Knief
  3. Institute of Vertebrate Biology, Czech Academy of Sciences, Brno, 603 65, Czech Republic

    • Pavlína Opatová
    • , Jana Albrechtová
    •  & Tomáš Albrecht
  4. Faculty of Science, Charles University, Prague, 128 44, Czech Republic

    • Pavlína Opatová
    • , Jana Albrechtová
    •  & Tomáš Albrecht
  5. Institute of Clinical Molecular Biology, Christian-Albrechts-University, Kiel, 24105, Germany

    • Michael Wittig
    •  & Andre Franke

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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Wolfgang Forstmeier.

Electronic supplementary material

  1. 1.

    Supplementary Information

    Supplementary Figures 1–4, Supplementary Tables 1–10, Supplementary References