-by- Regulatory Divergence Causes the Asymmetric Lethal Effects of an Ancestral Hybrid Incompatibility Gene

English version České info

The Dobzhansky and Muller (D-M) model explains the evolution of hybrid incompatibility (HI) through the interaction between lineage-specific derived alleles at two or more loci. In agreement with the expectation that HI results from functional divergence, many protein-coding genes that contribute to incompatibilities between species show signatures of adaptive evolution, including Lhr, which encodes a heterochromatin protein whose amino acid sequence has diverged extensively between Drosophila melanogaster and D. simulans by natural selection. The lethality of D. melanogaster/D. simulans F1 hybrid sons is rescued by removing D. simulans Lhr, but not D. melanogaster Lhr, suggesting that the lethal effect results from adaptive evolution in the D. simulans lineage. It has been proposed that adaptive protein divergence in Lhr reflects antagonistic coevolution with species-specific heterochromatin sequences and that defects in LHR protein localization cause hybrid lethality. Here we present surprising results that are inconsistent with this coding-sequence-based model. Using Lhr transgenes expressed under native conditions, we find no evidence that LHR localization differs between D. melanogaster and D. simulans, nor do we find evidence that it mislocalizes in their interspecific hybrids. Rather, we demonstrate that Lhr orthologs are differentially expressed in the hybrid background, with the levels of D. simulans Lhr double that of D. melanogaster Lhr. We further show that this asymmetric expression is caused by cis-by-trans regulatory divergence of Lhr. Therefore, the non-equivalent hybrid lethal effects of Lhr orthologs can be explained by asymmetric expression of a molecular function that is shared by both orthologs and thus was presumably inherited from the ancestral allele of Lhr. We present a model whereby hybrid lethality occurs by the interaction between evolutionarily ancestral and derived alleles.

Vyšlo v časopise: -by- Regulatory Divergence Causes the Asymmetric Lethal Effects of an Ancestral Hybrid Incompatibility Gene. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002597
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002597

Souhrn

Zdroje

1. DobzhanskyT 1937 Genetics and the origin of species New York Columbia Univ. Press

2. MullerHJ 1940 Bearing of the Drosophila work on systematics. HuxleyJS The new systematics Oxford Clarendon Press 185 268

3. MaheshwariSBarbashDA 2011 The genetics of hybrid incompatibilities. Annu Rev Genet 45 331 355

4. PresgravesDC 2010 The molecular evolutionary basis of species formation. Nat Rev Genet 11 175 180

5. BayesJJMalikHS 2009 Altered heterochromatin binding by a hybrid sterility protein in Drosophila sibling species. Science 326 1538 1541

6. FerreePMBarbashDA 2009 Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7 e1000234 doi:10.1371/journal.pbio.1000234

7. BrownJDO'NeillRJ 2010 Chromosomes, conflict, and epigenetics: chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11 291 316

8. JohnsonNA 2010 Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26 317 325

9. MullerHJ 1942 Isolating mechanisms, evolution and temperature. Biol Symp 6 71 125

10. CattaniMVPresgravesDC 2009 Genetics and lineage-specific evolution of a lethal hybrid incompatibility between Drosophila mauritiana and its sibling species. Genetics 181 1545 1555

11. ChenJDingJOuyangYDuHYangJ 2008 A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci U S A 105 11436 11441

12. ChouJYHungYSLinKHLeeHYLeuJY 2010 Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol 8 e1000432 doi:10.1371/journal.pbio.1000432

13. GrazeRMMcIntyreLMMainBJWayneMLNuzhdinSV 2009 Regulatory divergence in Drosophila melanogaster and D. simulans, a genomewide analysis of allele-specific expression. Genetics 183 547 561

14. McManusCJCoolonJDDuffMOEipper-MainsJGraveleyBRWittkoppPJ 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res 20 816 825

15. SturtevantAH 1920 Genetic studies on Drosphila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5 488 500

16. BrideauNJFloresHAWangJMaheshwariSWangXBarbashDA 2006 Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 1292 1295

17. HutterPAshburnerM 1987 Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327 331 333

18. WatanabeTK 1979 A gene that rescues the lethal hybrids between Drosophila melanogaster and D. simulans. Jpn J Genet 54 325 331

19. BarbashDASiinoDFTaroneAMRooteJ 2003 A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci U S A 100 5302 5307

20. GreilFde WitEBussemakerHJvan SteenselB 2007 HP1 controls genomic targeting of four novel heterochromatin proteins in Drosophila. EMBO J 26 741 751

21. BrideauNJBarbashDA 2011 Functional conservation of the Drosophila hybrid incompatibility gene Lhr. BMC Evol Biol 11 57

22. GrothACFishMNusseRCalosMP 2004 Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166 1775 1782

23. SánchezLDübendorferA 1983 Development of imaginal discs from lethal hybrids between Drosophila melanogaster and Drosophila mauritiana. Roux's Arch Dev Biol 192 48 50

24. KellumRRaffJWAlbertsBM 1995 Heterochromatin protein 1 distribution during development and during the cell cycle in Drosophila embryos. J Cell Sci 108 1407 1418

25. EbertALeinSSchottaGReuterG 2006 Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res 14 377 392

26. HsiehTBrutlagD 1979 Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol 135 465 481

27. KäsELaemmliUK 1992 In vivo topoisomerase II cleavage of the Drosophila histone and satellite III repeats: DNA sequence and structural characteristics. EMBO J 11 705 716

28. LoheARHillikerAJRobertsPA 1993 Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics 134 1149 1174

29. AbadJPCarmenaMBaarsSSaundersRDGloverDM 1992 Dodeca satellite: a conserved G+C-rich satellite from the centromeric heterochromatin of Drosophila melanogaster. Proc Natl Acad of Sci U S A 89 4663

30. CarmenaMAbadJPVillasanteAGonzalezC 1993 The Drosophila melanogaster dodeca satellite sequence is closely linked to the centromere and can form connections between sister chromatids during mitosis. J Cell Sci 105 41 50

31. LandryCRWittkoppPJTaubesCHRanzJMClarkAGHartlDL 2005 Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. Genetics 171 1813 1822

32. PresgravesDC 2003 A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163 955 972

33. LoheARobertsP 1988 Evolution of satellite DNA sequences in Drosophila. VermaRS Heterochromatin, Molecular and Structural Aspects Cambridge Cambridge Univ. Press 148 186

34. OrrHAMaddenLDCoyneJAGoodwinRHawleyRS 1997 The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145 1031 1040

35. BolkanBJBookerRGoldbergMLBarbashDA 2007 Developmental and cell cycle progression defects in Drosophila hybrid males. Genetics 177 2233 2241

36. TakahasiKRMatsuoTTakano-Shimizu-KounoT 2011 Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc Natl Acad Sci U S A 108 15276 15281

37. BarbashDAAwadallaPTaroneAM 2004 Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol 2 e142 doi:10.1371/journal.pbio.0020142

38. OliverPLGoodstadtLBayesJJBirtleZRoachKC 2009 Accelerated evolution of the Prdm9 speciation gene across diverse metazoan taxa. PLoS Genet 5 e1000753 doi:10.1371/journal.pgen.1000753

39. TingCTTsaurSCWuMLWuCI 1998 A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282 1501 1504

40. TweedieSAshburnerMFallsKLeylandPMcQuiltonP 2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37 D555 D559

41. PrigentSRMatsubayashiHYamamotoMT 2009 Transgenic Drosophila simulans strains prove the identity of the speciation gene Lethal hybrid rescue. Genes Genet Syst 84 353 360

42. BischofJMaedaRKHedigerMKarchFBaslerK 2007 An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 104 3312 3317

43. VenkenKJHeYHoskinsRABellenHJ 2006 P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314 1747 1751

44. FiumeraACDumontBLClarkAG 2005 Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics 169 243 257

45. ArunaSFloresHABarbashDA 2009 Reduced fertility of Drosophila melanogaster Hybrid male rescue (Hmr) mutant females is partially complemented by Hmr orthologs from sibling species. Genetics 181 1437 1450

46. AbràmoffMDMagalhãesPJRamSJ 2004 Image processing with ImageJ. Biophotonics international 11 36 42

47. BonaccorsiSLoheA 1991 Fine mapping of satellite DNA sequences along the Y chromosome of Drosophila melanogaster: relationships between satellite sequences and fertility factors. Genetics 129 177 189

48. StolcVGauharZMasonCHalaszGvan BatenburgMF 2004 A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306 655 660