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Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions

Nature Ecology & Evolution volume 2, pages 705–712 (2018)Cite this article

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Abstract

Males and females have different fitness optima but share the vast majority of their genomes, causing an inherent genetic conflict between the two sexes that must be resolved to achieve maximal population fitness. We show that two tandem duplicate genes found specifically in Drosophila melanogaster are sexually antagonistic, but rapidly evolved sex-specific functions and expression patterns that mitigate their antagonistic effects. We use copy-specific knockouts and rescue experiments to show that Apollo (Apl) is essential for male fertility but detrimental to female fertility, in addition to its important role in development, while Artemis (Arts) is essential for female fertility but detrimental to male fertility. Further analyses show that Apl and Arts have essential roles in spermatogenesis and oogenesis. These duplicates formed ~200,000 years ago, underwent a strong selective sweep and lost most expression in the antagonized sex. These data provide direct evidence that gene duplication allowed rapid mitigation of sexual conflict by allowing Apl and Arts to evolve essential sex-specific reproductive functions and complementary expression in male and female gonads.

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Fig. 1: Apl and Arts are D. melanogaster-specific duplicate genes.
Fig. 2: Apl and Arts CRISPR–Cas9 knockouts and their viability effects.
Fig. 3: Apl and Arts have sex-specific essential functions and are both sexually antagonistic.
Fig. 4: Expression pattern evolution of Apl, Arts and their homologues across Drosophila.
Fig. 5: Apl knockout prevents spermatid individualization.
Fig. 6: Arts knockouts disrupt actin networks required for egg elongation.

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Acknowledgements

We thank R. Renkawitz-Pohl for providing antibodies; S. Horne-Badovinac, C. Stevenson, T. Davis and I. Rebay for help with staining, microscopy and discussion; G.Y.-C. Lee for advice on population genomics analyses; and members of the Long lab, M. Kreitman, R. Hudson, E. Ferguson and L. Harshman for valuable discussion. N.W.V. was supported by the National Institutes of Health (NIH) Genetics and Regulation Training Grant T32GM007197 and a National Science Foundation (NSF) Graduate Research Fellowship. M.L. was supported by NSF1026200, NIH R01GM100768-01A1 and NIH R01GM116113.

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  1. Department of Ecology and Evolution, The University of Chicago, Chicago, IL, USA

    Nicholas W. VanKuren & Manyuan Long

  2. Committee on Genetics, Genomics and Systems Biology, The University of Chicago, Chicago, IL, USA

    Nicholas W. VanKuren & Manyuan Long

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  1. Nicholas W. VanKuren
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N.W.V. and M.L. designed the study. N.W.V. collected and analysed data with M.L. N.W.V. and M.L. wrote the manuscript.

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Correspondence to Nicholas W. VanKuren or Manyuan Long.

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VanKuren, N.W., Long, M. Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol 2, 705–712 (2018). https://doi.org/10.1038/s41559-018-0471-0

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