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Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions

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.

References

  1. 1.

    Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980).

    Article  Google Scholar 

  2. 2.

    Partridge, L. & Hurst, L. D. Sex and conflict. Science 281, 2003–2008 (1998).

    CAS  Article  Google Scholar 

  3. 3.

    Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009).

    Article  Google Scholar 

  4. 4.

    Parsch, J. & Ellegren, H. The evolutionary causes and consequences of sex-biased gene expression. Nat. Rev. Genet. 14, 83–87 (2013).

    CAS  Article  Google Scholar 

  5. 5.

    Gallach, M. & Betrán, E. Intralocus sexual conflict resolved through gene duplication. Trends Ecol. Evol. 26, 222–228 (2011).

    Article  Google Scholar 

  6. 6.

    Connallon, T. & Clark, A. G. The resolution of sexual antagonism by gene duplication. Genetics 187, 919–937 (2011).

    Article  Google Scholar 

  7. 7.

    Wyman, M. J., Cutter, A. D. & Rowe, L. Gene duplication in the evolution of sexual dimorphism. Evolution 66, 1556–1566 (2012).

    Article  Google Scholar 

  8. 8.

    Ohno, S. Evolution by Gene Duplication (Springer, Berlin, 1970).

  9. 9.

    Innan, H. & Kondrashov, F. The evolution of gene duplications: classifying and distinguishing between models. Nat. Rev. Genet. 11, 97–108 (2010).

    CAS  Article  Google Scholar 

  10. 10.

    Long, M., VanKuren, N. W., Chen, S. & Vibranovski, M. D. New gene evolution: little did we know. Annu. Rev. Genet. 47, 307–333 (2013).

    CAS  Article  Google Scholar 

  11. 11.

    Chippindale, A. K., Gibson, J. R. & Rice, W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl Acad. Sci. USA 98, 1671–1675 (2001).

    CAS  Article  Google Scholar 

  12. 12.

    Morrow, E. H., Stewart, A. D. & Rice, W. R. Assessing the extent of genome-wide intralocus sexual conflict via experimentally enforced gender-limited selection. J. Evol. Biol. 21, 1046–1054 (2008).

    CAS  Article  Google Scholar 

  13. 13.

    Innocenti, P. & Morrow, E. H. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 8, e1000335 (2010).

    Article  Google Scholar 

  14. 14.

    Obbard, D. J. et al. Estimating divergence dates and substitution rates in the Drosophila phylogeny. Mol. Biol. Evol. 29, 3459–3473 (2012).

    CAS  Article  Google Scholar 

  15. 15.

    Keightley, P. D. et al Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. Genome Res. 19, 1195–1201 (2009).

  16. 16.

    Rogers, R. L. & Hartl, D. L. Chimeric genes as a source of rapid evolution in Drosophila melanogaster. Mol. Biol. Evol. 29, 517–29 (2012).

    CAS  Article  Google Scholar 

  17. 17.

    Hudson, R. R., Kreitman, M. & Aguadé, M. A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Ford, M. J. & Aquadro, C. F. Selection on X-linked genes during speciation in the Drosophila athabasca complex. Genetics 144, 689–703 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Timinszky, G. et al. The importin-β P446L dominant-negative mutant protein loses RanGTP binding ability and blocks the formation of intact nuclear envelope. J. Cell Sci. 115, 1675–1687 (2002).

    CAS  Google Scholar 

  20. 20.

    Gorlich, D., Seewald, M. J. & Ribbeck, K. Characterization of Ran-driven cargo transport and the RanGTPase system by kinetic measurements and computer simulation. EMBO J. 22, 1088–1100 (2003).

    Article  Google Scholar 

  21. 21.

    Harel, A. & Forbes, D. J. Importin-β: conducting a much larger cellular symphony. Mol. Cell 16, 319–330 (2004).

    CAS  Google Scholar 

  22. 22.

    Gates, J. Drosophila egg chamber elongation: insights into how tissues and organs are shaped. Fly 6, 213–227 (2012).

    CAS  Article  Google Scholar 

  23. 23.

    Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS  Article  Google Scholar 

  24. 24.

    Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984).

    Article  Google Scholar 

  25. 25.

    Boughman, J. W. in The Princeton Guide to Evolution (eds Losos, J. B. et al.) 520–528 (Princeton University Press, Princeton, 2014).

  26. 26.

    Pavlicev, M. & Wagner, G. P. A model of developmental evolution: selection, pleiotropy and compensation. Trends Ecol. Evol. 27, 316–322 (2012).

    Article  Google Scholar 

  27. 27.

    Zera, A. J. & Harshman, L. G. The physiology of life history tradeoffs in animals. Annu. Rev. Ecol. Syst. 32, 95–126 (2001).

    Article  Google Scholar 

  28. 28.

    Harshman, L. G. & Hoffmann, A. A. Laboratory selection experiments in Drosophila: what do they really tell us? Trends Ecol. Evol. 15, 32–36 (2000).

    CAS  Article  Google Scholar 

  29. 29.

    Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D. & Hartl, D. L. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300, 1742–1745 (2003).

    CAS  Article  Google Scholar 

  30. 30.

    Ellegren, H. & Parsch, J. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 8, 689–698 (2007).

    CAS  Article  Google Scholar 

  31. 31.

    Zhou, Q. et al. On the origin of new genes in Drosophila. Genome Res. 18, 1446–1455 (2008).

    CAS  Article  Google Scholar 

  32. 32.

    Zhang, Y. E., Vibranovski, M. D., Krinsky, B. H. & Long, M. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 20, 1526–1533 (2010).

    CAS  Article  Google Scholar 

  33. 33.

    Chen, S. et al. Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila. Cell Rep. 1, 118–132 (2012).

    CAS  Article  Google Scholar 

  34. 34.

    Rogers, R. L. et al. Landscape of standing variation for tandem duplications in Drosophila yakuba and Drosophila simulans. Mol. Biol. Evol. 31, 1750–1766 (2014).

    CAS  Article  Google Scholar 

  35. 35.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    CAS  Article  Google Scholar 

  36. 36.

    Pool, J. et al. Population genomics of sub-saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet. 8, e1003080 (2012).

    Article  Google Scholar 

  37. 37.

    Dietzl, G. et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151–156 (2007).

  38. 38.

    Green, E. W., Fedele, G., Giorgini, F. & Kyriacou, C. P. A Drosophila RNAi collection is subject to dominant phenotypic effects. Nat. Methods 11, 222–223 (2014).

    CAS  Article  Google Scholar 

  39. 39.

    Bassett, A. & Liu, J. L. CRISPR/Cas9 mediated genome engineering in Drosophila. Methods 69, 128–136 (2014).

    CAS  Article  Google Scholar 

  40. 40.

    flyCRISPR Optimal Target Finder (University of Wisconsin, accessed 1 January 2016); http://tools.flycrispr.molbio.wisc.edu/targetFinder/

  41. 41.

    Port, F., Chen, H.-M., Lee, T. & Bullock, S. L. Optimized CRISPR/Cas tools for efficient germline and somatic genome engineering in Drosophila. Proc. Natl Acad. Sci. USA 111, E2967–E2976 (2014).

    CAS  Article  Google Scholar 

  42. 42.

    Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–360 (2012).

    CAS  Article  Google Scholar 

  43. 43.

    Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

    Article  Google Scholar 

  44. 44.

    Trapnell, C. et al. Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol. 31, 46–53 (2013).

    CAS  Article  Google Scholar 

  45. 45.

    Kibanov, M. V., Kotov, A. A. & Olenina, L. V. Multicolor fluorescence imaging of whole-mount Drosophila testes for studying spermatogenesis. Anal. Biochem. 436, 55–64 (2013).

    CAS  Article  Google Scholar 

  46. 46.

    Rathke, C. et al. Distinct functions of Mst77F and protamines in nuclear shaping and chromatin condensation during Drosophila spermiogenesis. Eur. J. Cell Biol. 89, 326–338 (2010).

    CAS  Article  Google Scholar 

  47. 47.

    McKenna, A. et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    CAS  Article  Google Scholar 

  48. 48.

    Van der Auwera, G. A. et al. in Current Protocols in Bioinformatics Vol. 43, 11.10.1–11.10.33 (John Wiley & Sons, 2013).

  49. 49.

    Langley, C. H. et al. Genomic variation in natural populations of Drosophila melanogaster. Genetics 192, 533–598 (2012).

    CAS  Article  Google Scholar 

  50. 50.

    Blanchette, M. et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708–715 (2004).

    CAS  Article  Google Scholar 

  51. 51.

    Harris, R. S. Improved Pairwise Alignment of Genomic DNA. PhD thesis, Pennsylvania State University (2007).

  52. 52.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Abascal, F., Zardoya, R. & Telford, M. J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38, 7–13 (2010).

    Article  Google Scholar 

  54. 54.

    Welch, B. L. The generalization of ‘Student’s’ problem when several different population variances are involved. Biometrika 34, 28–35 (1947).

    CAS  Google Scholar 

  55. 55.

    Shapiro, S. S. & Wilk, M. B. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611 (1965).

    Article  Google Scholar 

  56. 56.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2004).

  57. 57.

    van der Linde, K., Houle, D., Spicer, D. S. & Steppan, S. J. A supermatrix-based molecular phylogeny of the family Drosophilidae. Genet. Res. 92, 25–38 (2010).

    Article  Google Scholar 

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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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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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