Article

A sex-linked supergene controls sperm morphology and swimming speed in a songbird

  • Nature Ecology & Evolution 111681176 (2017)
  • doi:10.1038/s41559-017-0235-2
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Abstract

Sperm competition is an important selective force in many organisms. As a result, sperm have evolved to be among the most diverse cells in the animal kingdom. However, the relationship between sperm morphology, sperm motility and fertilization success is only partially understood. The extent to which between-male variation is heritable is largely unknown, and remarkably few studies have investigated the genetic architecture of sperm traits, especially sperm morphology. Here we use high-density genotyping and gene expression profiling to explore the considerable sperm trait variation that exists in the zebra finch Taeniopygia guttata. We show that nearly all of the genetic variation in sperm morphology is caused by an inversion polymorphism on the Z chromosome acting as a ‘supergene’. These results provide a striking example of two evolutionary genetic predictions. First, that in species where females are the heterogametic sex, genetic variation affecting sexually dimorphic traits will accumulate on the Z chromosome. Second, recombination suppression at the inversion allows beneficial dominant alleles to become fixed on whichever haplotype they first arise, without being exchanged onto other haplotypes. Finally, we show that the inversion polymorphism will be stably maintained by heterozygote advantage, because heterozygous males have the fastest and most successful sperm.

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Acknowledgements

We thank L. Gregory, G. Newsome and P. Young for help with animal care. G. van der Horst and J. Mossman provided CASA training and advice. R. Tucker and L. Ottaway assisted with DNA extractions. S. Manley and E. McLaren assisted with sperm measurements. C. Bloor, A. Davassi and G. Scopes, all of Affymetrix, provided help with the SNP chip design and quality control. A. Downing, K. Gharbi, H. Gunter, J. Risse, R. Talbot and U. Trivedi of Edinburgh Genomics assisted with SNP genotyping and gene expression microarray scanning. The study was funded by grants BB/I02185X/1 from the Biotechnology and Biological Sciences Research Council (to J.S.) and ERC-2010-AdG from the European Research Council (to T.R.B.), and by a PhD studentship from the Natural Environment Research Council (to C.B.).

Author information

Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK

    • Kang-Wook Kim
    • , Clair Bennison
    • , Nicola Hemmings
    • , Lola Brookes
    • , Terry Burke
    • , Tim R. Birkhead
    •  & Jon Slate
  2. Department of Biological Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    • Laura L. Hurley
    •  & Simon C. Griffith

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Contributions

C.B., N.H. and L.B. collected and measured sperm data. C.B., N.H. and T.R.B. designed and implemented the selection-line experiments. K.-W.K. designed the SNP chip and performed molecular work. K.-W.K. and J.S. analysed the data. T.R.B. managed the long-term study of zebra finches in Sheffield. L.L.H. and S.C.G. collected the samples from the Australian population. K.-W.K. and J.S. wrote the paper with contributions from all other authors. T.B., T.R.B. and J.S. conceived the study.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Kang-Wook Kim or Jon Slate.

Supplementary information

  1. 1.

    Supplementary Information

    Supplementary Tables 1–4 and Supplementary Figures 1–6

  2. 2.

    Supplementary Data Set 1

    Summary of GWAS, eQTL and eigenGWAS analyses

  3. 3.

    Supplementary Data Set 2

    Summary of gene expression in testes

  4. 4.

    Supplementary Video 1

    Video of motile sperm of alternative karyotypes