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Allelic asymmetry of the Lethal hybrid rescue (Lhr) gene expression in the hybrid between Drosophila melanogaster and D. simulans: confirmation by using genetic variations of D. melanogaster

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Abstract

In the cross between Drosophila melanogaster females and D. simulans males, hybrid males die at the late larval stage, and the sibling females also die at later stages at high temperatures. Removing the D. simulans allele of the Lethal hybrid rescue gene (Lhr sim) improves the hybrid incompatibility phenotypes. However, the loss-of-function mutation of Lhr sim (Lhr sim0) does not rescue the hybrid males in crosses with several D. melanogaster strains. We first describe the genetic factor possessed by the D. melanogaster strains. It has been suggested that removing the D. melanogaster allele of Lhr (Lhr mel), that is Lhr mel0, does not have the hybrid male rescue effect, contrasting to Lhr sim0. Because the expression level of the Lhr gene is known to be Lhr sim > Lhr mel in the hybrid, Lhr mel0 may not lead to enough of a reduction in total Lhr expression. Then, there is a possibility that the D. melanogaster factor changes the expression level to Lhr sim < Lhr mel. But in fact, the expression level was Lhr sim > Lhr mel in the hybrid irrespectively of the presence of the factor. At last, we showed that Lhr mel0 slightly improves the viability of hybrid females, which was not realized previously. All of the present results are consistent with the allelic asymmetry model of the Lhr gene expression in the hybrid.

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References

  • Aruna S, Flores HA, Barbash DA (2009) Reduced fertility of Drosophila hybrid male rescue (Hmr) mutant females is partially complemented by Hmr orthologs from sibling species. Genetics 181:1437–1450

    Article  CAS  PubMed  Google Scholar 

  • Barbash DA (2010) Genetic testing of the hypothesis that hybrid male lethality results from a failure in dosage compensation. Genetics 184:313–316

    Article  CAS  PubMed  Google Scholar 

  • Barbash DA, Ashburner M (2003) A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics 163:217–226

    CAS  PubMed  Google Scholar 

  • Barbash DA, Awadalla P, Tarone AM (2004) Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol 2:e142

    Article  PubMed Central  PubMed  Google Scholar 

  • Barbash DA, Lorigan JG (2007) Lethality in Drosophila melanogaster/Drosophila simulans species hybrids is not associated with substantial transcriptional misregulation. J Exp Zool B Mol Dev Evol 308B:74–84

    Article  CAS  Google Scholar 

  • Barbash DA, Roote J, Ashburner M (2000) The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154:1747–1771

    CAS  PubMed  Google Scholar 

  • Barbash DA, Siino DF, Tarone AM, Roote J (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100:5302–5307

    Article  CAS  PubMed  Google Scholar 

  • Bolkan BJ, Booker R, Goldberg ML, Barbash DA (2007) Developmental and cell cycle progression defects in Drosophila hybrid males. Genetics 177:2233–2241

    Article  CAS  PubMed  Google Scholar 

  • Brideau NJ, Barbash DA (2011) Functional conservation of the Drosophila hybrid incompatibility gene Lhr. BMC Evol Biol 11:57

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, Barbash DA (2006) Two Dobzhansky–Muller genes interact to cause hybrid lethality in Drosophila. Science 314:1292–1295

    Article  CAS  PubMed  Google Scholar 

  • Davis AW, Roote J, Morley T, Sawamura K, Herrmann S, Ashburner M (1996) Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380:157–159

    Article  CAS  PubMed  Google Scholar 

  • Granadino B, Penalva LOF, Sánchez L (1996) Indirect evidence of alteration in the expression of the rDNA genes in interspecific hybrids between Drosophila melanogaster and Drosophila simulans. Mol Gen Genet 250:89–96

    CAS  PubMed  Google Scholar 

  • Hadorn E (1961) Zur Autonomie und Phasenspezifität der Letalität von Bastarden zwischen Drosophila melanogaster und Drosophila simulans. Rev Suisse Zool 68:197–207

    Google Scholar 

  • Hutter P, Ashburner M (1987) Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327:331–333

    Article  CAS  PubMed  Google Scholar 

  • Hutter P, Roote J, Ashburner M (1990) A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124:909–920

    CAS  PubMed  Google Scholar 

  • Kerkis J (1933) Einfluss der Temperatur auf die Entwicklung der Hybriden von Drosophila melanogaster × Drosophila simulans. Wilhelm Roux’ Arch Entwicklungsmech Org 130:1–10

    Article  Google Scholar 

  • Lee WH (1978) Temperature sensitive viability of hybrid between Drosophila melanogaster and D. simulans. Jpn J Genet 53:339–344

    Article  Google Scholar 

  • Lohe AR, Roberts PA (1990) An unusual Y chromosome of Drosophila simulans amplified rDNA spacer without rRNA genes. Genetics 125:399–406

    CAS  PubMed  Google Scholar 

  • Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45:331–355

    Article  CAS  PubMed  Google Scholar 

  • Maheshwari S, Barbash DA (2012a) An indel polymorphism in the hybrid incompatibility gene Lethal hybrid rescue of Drosophila is functionally relevant. Genetics 192:683–691

    Article  CAS  PubMed  Google Scholar 

  • Maheshwari S, Barbash DA (2012b) Cis-by-trans regulatory divergence causes the asymmetric lethal effects of an ancestral hybrid incompatibility gene. PLoS Genet 8:e1002597

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maheshwari S, Wang J, Barbash DA (2008) Recurrent positive selection of the Drosophila hybrid incompatibility gene Hmr. Mol Biol Evol 25:2421–2430

    Article  CAS  PubMed  Google Scholar 

  • Nolte V, Weigel D, Schlötterer C (2008) The impact of shared ancestral variation on hybrid male lethality—a 16 codon indel in the Drosophila simulans Lhr gene. J Evol Biol 21:551–555

    Article  CAS  PubMed  Google Scholar 

  • Presgraves DC (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163:955–972

    CAS  PubMed  Google Scholar 

  • Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11:175–180

    Article  CAS  PubMed  Google Scholar 

  • Presgraves DC, Balagopalan L, Abmayr SM, Orr HA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423:715–718

    Article  CAS  PubMed  Google Scholar 

  • Prigent S, Matsubayashi H, Yamamoto MT (2009) Transgenic Drosophila simulans strains prove the identity of the speciation gene Lethal hybrid rescue. Genes Genet Syst 84:353–360

    Article  CAS  PubMed  Google Scholar 

  • Sawamura K (2012) Chromatin evolution and molecular drive in speciation. Int J Evol Biol 2012:301894

    PubMed Central  PubMed  Google Scholar 

  • Sawamura K, Taira T, Watanabe TK (1993a) Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosohila simulans. Genetics 133:299–305

    CAS  PubMed  Google Scholar 

  • Sawamura K, Watanabe TK, Yamamoto MT (1993b) Hybrid lethal systems in the Drosophila melanogaster species complex. Genetica 88:175–185

    Article  CAS  PubMed  Google Scholar 

  • Sawamura K, Yamamoto MT, Watanabe TK (1993c) Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of D. melanogaster. Genetics 133:307–313

    CAS  PubMed  Google Scholar 

  • Sawamura K, Maehara K, Mashino S, Kagesawa T, Kajiwara M, Matsuno K, Takahashi A, Takano-Shimizu T (2010) Introgression of Drosophila simulans Nuclear Pore Protein 160 in Drosophila simulans alone does not cause inviability but does cause female sterility. Genetics 186:669–676

    Article  CAS  PubMed  Google Scholar 

  • Sturtevant AH (1920) Genetic studies on Drosophila simulans. I Introduction. Hybrids with Drosophila melanogaster. Genetics 5:488–500

    CAS  PubMed  Google Scholar 

  • Tang S, Presgraves DC (2009) Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323:779–782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watanabe TK (1979) A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Jpn J Genet 54:325–331

    Article  Google Scholar 

  • Watanabe TK, Lee WH, Inoue Y, Kawanishi M (1977) Genetic variation of the hybrid crossability between Drosophila melanogaster and D. simulans. Jpn J Genet 52:1–8

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to the Bloomington, Kyoto, and Ehime Drosophila stock centers, T. Miyo, T. Orr-Weaver, J. Roote, and M. T. Yamamoto for providing fly strains. We thank J. Kitano, A. Ishikawa, and R. Niwa for facility help and technical advice. This work was partly supported by Grants-in-Aid for Scientific Research (21570001 and 24570001) to KS from the Japan Society for the Promotion of Science and NIG Collaborative Research Program (2012-A83) from the National Institute of Genetics to KS, TTS, and J. Kitano. Comments from two anonymous reviewers improved this report.

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Authors and Affiliations

  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan

    Mika Shirata, Quenta Araye, Kazunori Maehara & Sora Enya

  2. Drosophila Genetic Resource Center, Kyoto Institute of Technology, Kyoto, Japan

    Toshiyuki Takano-Shimizu

  3. Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

    Kyoichi Sawamura

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  1. Mika Shirata
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  2. Quenta Araye
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  3. Kazunori Maehara
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  4. Sora Enya
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  5. Toshiyuki Takano-Shimizu
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  6. Kyoichi Sawamura
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Correspondence to Kyoichi Sawamura.

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Shirata, M., Araye, Q., Maehara, K. et al. Allelic asymmetry of the Lethal hybrid rescue (Lhr) gene expression in the hybrid between Drosophila melanogaster and D. simulans: confirmation by using genetic variations of D. melanogaster . Genetica 142, 43–48 (2014). https://doi.org/10.1007/s10709-013-9752-3

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