Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila

  • 1.

    Sandler, L. & Novitski, E. Meiotic drive as an evolutionary force. Am. Nat. 91, 105–110 (1957).

    Article 

    Google Scholar
     

  • 2.

    Lindholm, A. K. et al. The ecology and evolutionary dynamics of meiotic drive. Trends Ecol. Evol. 31, 315–326 (2016).

    Article 
    PubMed 

    Google Scholar
     

  • 3.

    Lyttle, T. W. Segregation distorters. Annu. Rev. Genet. 25, 511–557 (1991).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 4.

    Lyttle, T. W. Cheaters sometimes prosper: distortion of Mendelian segregation by meiotic drive. Trends Genet. 9, 205–210 (1993).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 5.

    Presgraves, D. C. in Sperm Biology: An Evolutionary Perspective (eds Birkhead, T. R. et al.) Ch. 12, 472–506 (Elsevier Press, 2008).

  • 6.

    Hartl, D. L. Genetic dissection of segregation distortion. I. Suicide combinations of SD genes. Genetics 76, 477–486 (1974).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 7.

    Charlesworth, B. & Hartl, D. L. Population dynamics of the segregation distorter polymorphism of Drosophila melanogaster. Genetics 89, 171–192 (1978).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 8.

    Hamilton, W. D. Extraordinary sex ratios. Science 156, 477–488 (1967).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 9.

    Hurst, L. D. & Pomiankowski, A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane’s rule and related phenomena. Genetics 128, 841–858 (1991).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 10.

    Frank, S. H. Divergence of meiotic drive-suppressors as an explanation for sex-biased hybrid sterility and inviability. Evolution 45, 262–267 (1991).

    PubMed 

    Google Scholar
     

  • 11.

    Gershenson, S. A new sex ratio abnormality in Drosophila obscura. Genetics 13, 488–507 (1928).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 12.

    Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, 1930).

  • 13.

    Jaenike, J. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 32, 25–49 (2001).

    Article 

    Google Scholar
     

  • 14.

    Vaz, S. C. & Carvalho, A. B. Evolution of autosomal suppression of the sex-ratio trait in Drosophila. Genetics 166, 265–277 (2004).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 15.

    Hall, D. W. Meiotic drive and sex chromosome cycling. Evolution 58, 925–931 (2004).

    Article 
    PubMed 

    Google Scholar
     

  • 16.

    Hartl, D. L. Modifier theory and meiotic drive. Theor. Popul. Biol. 7, 168–174 (1975).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 17.

    Thomson, G. J. & Feldman, M. W. Population genetics of modifiers of meiotic drive. II. Linkage modification in the Segregation Distorter system. Theor. Popul. Biol. 5, 155–162 (1974).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 18.

    Bastide, H., Gerard, P. R., Ogereau, D., Cazemajor, M. & Montchamp-Moreau, C. Local dynamics of a fast-evolving sex-ratio system in Drosophila simulans. Mol. Ecol. 22, 5352–5367 (2013).

    Article 
    PubMed 

    Google Scholar
     

  • 19.

    Haig, D. & Grafen, A. Genetic scrambling as a defence against meiotic drive. J. Theor. Biol. 153, 531–558 (1991).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 20.

    Burt, A. & Trivers, R. A. Genes in Conflict (Harvard Univ. Press, 2006).

  • 21.

    Meiklejohn, C. D. & Tao, Y. Genetic conflict and sex chromosome evolution. Trends Ecol. Evol. 25, 215–223 (2010).

    Article 
    PubMed 

    Google Scholar
     

  • 22.

    Bachtrog, D. The Y chromosome as a battleground for intragenomic conflict. Trends Genet. 36, 510–522 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 23.

    Tao, Y. et al. A sex-ratio meiotic drive system in Drosophila simulans. II: An X-linked distorter. Public Libr. Sci. Biol. 5, e293 (2007).


    Google Scholar
     

  • 24.

    Tao, Y., Masly, J. P., Araripe, L., Ke, Y. & Hartl, D. L. A sex-ratio meiotic drive system in Drosophila simulans. I: An autosomal suppressor. Public Libr. Sci. Biol. 5, e292 (2007).


    Google Scholar
     

  • 25.

    Lin, C. J. et al. The hpRNA/RNAi pathway is essential to resolve intragenomic conflict in the Drosophila male germline. Dev. Cell 46, 316–326 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 26.

    Kingan, S. B., Garrigan, D. & Hartl, D. L. Recurrent selection on the Winters sex-ratio genes in Drosophila simulans. Genetics 184, 253–265 (2010).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 27.

    Meiklejohn, C. D. et al. Gene flow mediates the role of sex chromosome meiotic drive during complex speciation. eLife 7, e35468 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 28.

    Nolte, V., Pandey, R. V., Kofler, R. & Schlotterer, C. Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana. Genome Res. 23, 99–110 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 29.

    Garrigan, D., Kingan, S. B., Geneva, A. J., Vedanayagam, J. P. & Presgraves, D. C. Genome diversity and divergence in Drosophila mauritiana: multiple signatures of faster X evolution. Genome Biol. Evol. 6, 2444–2458 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 30.

    Tao, Y., Hartl, D. L. & Laurie, C. C. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc. Natl Acad. Sci. USA 98, 13183–13188 (2001).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 31.

    Chakraborty, M. et al. Evolution of genome structure in the Drosophila simulans species complex. Genome Res. 31, 380–396 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 32.

    Sproul, J. S. et al. Dynamic evolution of euchromatic satellites on the X chromosome in Drosophila melanogaster and the simulans clade. Mol. Biol. Evol. 37, 2241–2256 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 33.

    Joshi, S. S. & Meller, V. H. Satellite repeats identify X chromatin for dosage compensation in Drosophila melanogaster males. Curr. Biol. 27, 1393–1402 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 34.

    Garrigan, D. et al. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res. 22, 1499–1511 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 35.

    Kliman, R. M. et al. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156, 1913–1931 (2000).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 36.

    Miller, D., Brinkworth, M. & Iles, D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 139, 287–301 (2010).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 37.

    Gingell, L. F. & McLean, J. R. A protamine knockdown mimics the function of Sd in Drosophila melanogaster. G3 10, 2111–2115 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 38.

    Larracuente, A. M. & Presgraves, D. C. The selfish Segregation Distorter complex of Drosophila melanogaster. Genetics 192, 33–53 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 39.

    Wu, C.-I., Lyttle, T. W., Wu, M.-L. & Lin, G. F. Association between DNA satellite sequences and the responder of Segregation Distorter in D. melanogaster. Cell 54, 179–189 (1988).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 40.

    Thomas, J., Phillips, C. D., Baker, R. J. & Pritham, E. J. Rolling-circle transposons catalyze genomic innovation in a mammalian lineage. Genome Biol. Evol. 6, 2595–2610 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 41.

    Hurst, L. D. Is Stellate a relict meiotic driver? Genetics 130, 229–230 (1992).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 42.

    Cocquet, J. et al. The multicopy gene Sly represses the sex chromosomes in the male mouse germline after meiosis. PLoS Genet. 7, e1000244 (2009).

    Article 
    CAS 

    Google Scholar
     

  • 43.

    Kruger, A. N. et al. A neofunctionalized X-linked ampliconic gene family is essential for male fertility and equal sex ratio in mice. Curr. Biol. 29, 3699–3706 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 44.

    Hu, W. et al. A large gene family in fission yeast encodes spore killers that subvert Mendel’s law. eLife 6, e26057 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 45.

    Eickbush, M. T., Young, J. M. & Zanders, S. E. Killer meiotic drive and dynamic evolution of the wtf gene family. Mol. Biol. Evol. 36, 1201–1214 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 46.

    Vogan, A. A. et al. Combinations of Spok genes create multiple meiotic drivers in Podospora. eLife 8, e46454 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 47.

    Derome, N., Metayer, K., Montchamp-Moreau, C. & Veuille, M. Signature of selective sweep associated with the evolution of sex-ratio drive in Drosophila simulans. Genetics 1166, 1357–1366 (2004).

    Article 

    Google Scholar
     

  • 48.

    Presgraves, D. C., Gerard, P. R., Cherukuri, A. & Lyttle, T. W. Large-scale selective sweep among Segregation Distorter chromosomes in African populations of Drosophila melanogaster. PLoS Genet. 5, e1000463 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 49.

    Nam, K. et al. Extreme selective sweeps independently targeted the X chromosomes of the great apes. Proc. Natl Acad. Sci. USA 112, 6413–6418 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 50.

    Aravin, A. A. et al. Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr. Biol. 11, 1017–1027 (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar
     

  • 51.

    Daugherty, M. D. & Zanders, S. E. Gene conversion generates evolutionary novelty that fuels genetic conflicts. Curr. Opin. Genet. Dev. 58–59, 49–54 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 52.

    Beckmann, J. F., Sharma, G. D., Mendez, L., Chen, H. & Hochstrasser, M. The Wolbachia cytoplasmic incompatibility enzyme CidB targets nuclear import and protamine-histone exchange factors. eLife 8, e50026 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

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