Interspecific Tests of Allelism Reveal the Evolutionary Timing and Pattern of Accumulation of Reproductive Isolation Mutations

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The evolution of reproductive barriers between species, like inviability and sterility in hybrids, continues to fascinate and puzzle evolutionary biologists. However, very few studies have successfully identified the genes responsible for these barriers, or when the underlying mutations appeared during species' evolutionary history of divergence. Differentiating whether specific isolation-causing mutations evolved early versus late in the divergence history of lineages can reveal important insights into the mechanisms of speciation—how new species are formed. Here we infer the evolutionary timing of these loci using data on the chromosomal location of genes that cause reduced hybrid pollen and seed fertility among three species in the wild tomato group, and information on their evolutionary relationships. With genetic crosses that combine these sterility loci from different lineages, we evaluate whether sterility effects are due to the same mutational change(s)—earlier in the history of evolutionary divergence among these species—or to independent mutational changes—later in their evolutionary divergence. We show that most sterility loci separating species are unique to a single species pair, and most isolation-causing mutations arose on recent evolutionary branches. Our data are consistent with mathematical models that predict that these loci should ‘snowball’ between species as they diverge.

Vyšlo v časopise: Interspecific Tests of Allelism Reveal the Evolutionary Timing and Pattern of Accumulation of Reproductive Isolation Mutations. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004623
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004623

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Zdroje

1. DobzhanskyT (1936) Studies on hybrid sterility II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21 : 113–135.

2. MullerHJ (1942) Isolating mechanisms, evolution, and temperature. Biological Symposia 6 : 71–125.

3. OrrHA, TurelliM (2001) The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller incompatibilities. Evolution 55 : 1085–1094.

4. LiuYS, ZhuLH, SunJS, ChenY (2001) Mapping QTLs for defective female gametophyte development in an inter-subspecific cross in Oryza sativa L. Theoretical and Applied Genetics 102 : 1243–1251.

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

6. SlotmanM, della TorreA, PowellJR (2004) The genetics of inviability and male sterility in hybrids between Anopheles gambiae and An. arabiensis. Genetics 167 : 275–287.

7. MoyleLC, GrahamEB (2005) Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum. Genetics 169 : 355–373.

8. MaslyJP, PresgravesDC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biology 5 : 1890–1898.

9. MatsubaraK, AndoT, MizubayashiT, ItoS, YanoM (2007) Identification and linkage mapping of complementary recessive genes causing hybrid breakdown in an intraspecific rice cross. Theoretical and Applied Genetics 115 : 179–186.

10. LeppalaJ, SavolainenO (2011) Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsis lyrata subspecies. Evolution 65 : 2959–2972.

11. PhadnisN (2011) Genetic architecture of male sterility and segregation distortion in Drosophila pseudoobscura Bogota-USA Hybrids. Genetics 189 : 1001–U1428.

12. BalleriniES, BrothersAN, TangS, KnappSJ, BouckA, et al. (2012) QTL mapping reveals the genetic architecture of loci affecting pre -⁠ and post-zygotic isolating barriers in Louisiana Iris. BMC Plant Biology 12 : 91.

13. Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. In: Bassler BL, Lichten M, Schupbach G, editors. Annual Review Genetics, Vol 45. pp. 331–355.

14. SweigartAL, WillisJH (2012) Molecular evolution and genetics of postzygotic reproductive isolation in plants. F1000 Biology Reports 4 : 23.

15. OrrHA (1995) The population genetics of speciation -⁠ The evolution of hybrid incompatibilities. Genetics 139 : 1805–1813.

16. Gavrilets S (2004) Fitness landscapes and the origin of species. 1–432 p.

17. TurelliM, MoyleLC (2007) Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176 : 1059–1088.

18. PalmerME, FeldmanMW (2009) Dynamics of hybrid incompatibility in gene networks in a constant environment. Evolution 63 : 418–431.

19. WangRJ, AneC, PayseurBA (2013) The evolution of hybrid incompatibilities along a phylogeny. Evolution 67 : 2905–2922.

20. MoyleLC, PayseurBA (2009) Reproductive isolation grows on trees. Trends in Ecology & Evolution 24 : 591–598.

21. TingCT, TsaurSC, WuML, WuCI (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282 : 1501–1504.

22. BarbashDA, SiinoDF, TaroneAM, RooteJ (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 100 : 5302–5307.

23. PresgravesDC, BalagopalanL, AbmayrSM, OrrHA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423 : 715–719.

24. PresgravesDC, StephanW (2007) Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96. Molecular Biology and Evolution 24 : 306–314.

25. MaheshwariS, WangJ, BarbashDA (2008) Recurrent positive selection of the Drosophila hybrid incompatibility gene Hmr. Molecular Biology and Evolution 25 : 2421–2430.

26. TangS, PresgravesDC (2009) Evolution of the Drosophila Nuclear Pore Complex results in multiple hybrid incompatibilities. Science 323 : 779–782.

27. MoyleLC, NakazatoT (2008) Comparative genetics of hybrid incompatibility: Sterility in two Solanum species crosses. Genetics 179 : 1437–1453.

28. MatsubaraK, EbanaK, MizubayashiT, ItohS, AndoT, et al. (2011) Relationship between transmission ratio distortion and genetic divergence in intraspecific rice crosses. Molecular Genetics and Genomics 286 : 307–319.

29. WhiteMA, StubbingsM, DumontBL, PayseurBA (2012) Genetics and evolution of hybrid male sterility in house mice. Genetics 191 : 917–U473.

30. MoyleLC, NakazatoT (2010) Hybrid incompatibility “snowballs” between Solanum species. Science 329 : 1521–1523.

31. MatuteDR, ButlerIA, TurissiniDA, CoyneJA (2010) A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329 : 1518–1521.

32. CattaniMV, PresgravesDC (2009) Genetics and lineage-specific evolution of a lethal hybrid Incompatibility between Drosophila mauritiana and its sibling species. Genetics 181 : 1545–1555.

33. McDermottSR, NoorMAF (2011) Genetics of hybrid sterility among strains and species in the Drosophila pseudoobscura species group. Evolution 65 : 1969–1978.

34. HawleyRS, GillilandWD (2006) Sometimes the result is not the answer: the truths and the lies that come from using the complementation test. Genetics 174 : 5–15.

35. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77 : 71–94.

36. StamatakisA (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 : 2688–2690.

37. HaakDC, BallengerBA, MoyleLC (2014) No evidence for phylogenetic constraint on natural defense evolution among wild tomatoes. Ecology 95 : 1633–1641.

38. OrrHA, MaslyJP, PresgravesDC (2004) Speciation genes. Current Opinion in Genetics & Development 14 : 675–679.

39. RiesebergLH, BlackmanBK (2010) Speciation genes in plants. Annals of Botany 106 : 439–455.

40. MaslyJP, JonesCD, NoorMAF, LockeJ, OrrHA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313 : 1448–1450.

41. BikardD, PatelD, Le MetteC, GiorgiV, CamilleriC, et al. (2009) Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science 323 : 623–626.

42. MizutaY, HarushimaY, KurataN (2010) Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proceedings of the National Academy of Sciences of the United States of America 107 : 20417–20422.

43. WerthCR, WindhamMD (1991) A model for divergent, allopatric speciation of polyploid pteridophytes resulting from silencing of duplicate gene expression. American Naturalist 137 : 515–526.

44. LynchM, ForceAG (2000) The origin of interspecific genomic incompatibility via gene duplication. American Naturalist 156 : 590–605.

45. Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinauer Assoc., Inc. 545 p.

46. OrrHA (1998) The population genetics of adaptation: The distribution of factors fixed during adaptive evolution. Evolution 52 : 935–949.

47. WuCI, PalopoliMF (1994) Genetics of postmating reproductive isolation in animals. Annual Review of Genetics 28 : 283–308.

48. CabotEL, DavisAW, JohnsonNA, WuCI (1994) Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics 137 : 175–189.

49. PalopoliMF, WuCI (1994) Genetics of hybrid male-sterility between Drosophila sibling species -⁠ a complex web of epistasis is revealed in interspecific studies. Genetics 138 : 329–341.

50. OrrHA, IrvingS (2001) Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158 : 1089–1100.

51. BrideauNJ, FloresHA, WangJ, MaheshwariS, WangX, et al. (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 : 1292–1295.

52. BarbashDA (2007) Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila. Genetics 176 : 543–552.

53. LongY, ZhaoL, NiuB, SuJ, WuH, et al. (2008) Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proceedings of the National Academy of Sciences of the United States of America 105 : 18871–18876.

54. ChangAS, BennettSM, NoorMAF (2010) Epistasis among Drosophila persimilis factors conferring hybrid male sterility with D. pseudoobscura bogotana. PLoS One 5: e15377.

55. JohnsonNA (2010) Hybrid incompatibility genes: remnants of a genomic battlefield? Trends in Genetics 26 : 317–325.

56. WittkoppPJ, StewartEE, ArnoldLL, NeidertAH, HaerumBK, et al. (2009) Intraspecific polymorphism to interspecific divergence: Genetics of pigmentation in Drosophila. Science 326 : 540–544.

57. FergusonLC, MarojaL, JigginsCD (2011) Convergent, modular expression of ebony and tan in the mimetic wing patterns of Heliconius butterflies. Development Genes and Evolution 221 : 297–308.

58. WessingerCA, RausherMD (2012) Lessons from flower colour evolution on targets of selection. Journal of Experimental Botany 63 : 5741–5749.

59. ManceauM, DominguesVS, LinnenCR, RosenblumEB, HoekstraHE (2010) Convergence in pigmentation at multiple levels: mutations, genes and function. Philosophical Transactions of the Royal Society B-Biological Sciences 365 : 2439–2450.

60. LososJB (2011) Convergence, adaptation, and constraint. Evolution 65 : 1827–1840.

61. EshedY, ZamirD (1994) A genomic library of Lycopersicon pennellii in Lycopersicon esculentum -⁠ A tool for fine mapping of genes. Euphytica 79 : 175–179.

62. EshedY, ZamirD (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141 : 1147–1162.

63. MonforteAJ, TanksleySD (2000) Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: A tool for gene mapping and gene discovery. Genome 43 : 803–813.

64. Crawley MJ (2013) The R book. John Wiley and Sons, West Sussex, UK.

65. Falconer DS (1964) Introduction to quantitative genetics. Oliver and Boyd, Edinburgh, UK.