Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities

English version České info

Understanding the origin of species is one of the central challenges in evolutionary biology. It has been suggested that hybridization could generate new species because hybrids can display novel combinations of traits that induce reproductive isolation from their parental species (called “hybrid speciation”). Existing models predict that this should only occur in special cases, and indeed there have been only few well-supported examples. We describe a new model of hybrid reproductive isolation that results from selection against genetic incompatibilities in hybrids, which are predicted to be common. Simulations reveal that hybrid populations rapidly and frequently become isolated from parental species by fixing combinations of genes that hinder successful reproduction with parental species. We propose that this process could be an important mechanism for the formation of new species.

Vyšlo v časopise: Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005041
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005041

Souhrn

Zdroje

1. Arnold ML (2006) Evolution through genetic exchange. Oxford, U.K.: Oxford University Press.

2. Mallet J (2007) Hybrid speciation. Nature 446 : 279–283. 17361174

3. Nolte AW, Tautz D (2010) Understanding the onset of hybrid speciation. Trends Genet 26 : 54–58. doi: 10.1016/j.tig.2009.12.001 20044166

4. Schumer M, Rosenthal GG, Andolfatto P (2014) How common is homoploid hybrid speciation? Evolution 68 : 1553–1560. doi: 10.1111/evo.12399 24620775

5. Rieseberg LH, Vanfossen C, Desrochers AM (1995) Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 375 : 313–316.

6. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, et al. (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301 : 1211–1216. 12907807

7. Lexer C, Welch ME, Raymond O, Rieseberg LH (2003) The origin of ecological divergence in Helianthus paradoxus (Asteraceae): Selection on transgressive characters in a novel hybrid habitat. Evolution 57 : 1989–2000. 14575321

8. Mavarez J, Salazar CA, Bermingham E, Salcedo C, Jiggins CD, et al. (2006) Speciation by hybridization in Heliconius butterflies. Nature 441 : 868–871. 16778888

9. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH (2000) The likelihood of homoploid hybrid speciation. Heredity 84 : 441–451. 10849068

10. Schwarz D, Matta BM, Shakir-Botteri NL, McPheron BA (2005) Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436 : 546–549. 16049486

11. Schwarz D, Shoemaker KD, Botteri NL, McPheron BA (2007) A novel preference for an invasive plant as a mechanism for animal hybrid speciation. Evolution 61 : 245–256. 17348936

12. Duenez-Guzman EA, Mavarez J, Vose MD, Gavrilets S. (2009) Case studies and mathematical models of ecological speciation. 4. Hybrid speciation in butterflies in a jungle. Evolution. 63 : 2611–26. doi: 10.1111/j.1558-5646.2009.00756.x 19545268

13. Jiggins CD, Salazar C, Linares M, Mavarez J (2008) Hybrid trait speciation and Heliconius butterflies. Philos T Roy Soc B 363 : 3047–3054. doi: 10.1098/rstb.2008.0065 18579480

14. McCarthy EM, Asmussen MA, Anderson WW (1995) A theoretical assessment of recombinational speciation. Heredity 74 : 502–509.

15. Grant V (1971) Plant Speciation. New York: Columbia University Press.

16. Lai Z, Nakazato T, Salmaso M, Burke JM, Tang SX, et al. (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171 : 291–303. 16183908

17. Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. In: Brigham CA, Schwarz MW, editors. Population viability in plants: Conservation, management, and modeling of rare plants pp. 117–141.

18. Carr DE, Rieseberg LH, Abbott RJ (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations—Discussion. Philos T Roy Soc B 358 : 1147–1147.

19. Rieseberg LH, Widmer A, Arntz AM, Burke JM (2003) The genetic architecture necessary for transgressive segregation is common in both natural and domesticated populations. Philos T Roy Soc B 358 : 1141–1147. 12831480

20. Stelkens R, Seehausen O (2009) Genetic distance between species predicts novel trait expression in their hybrids. Evolution 63 : 884–897. doi: 10.1111/j.1558-5646.2008.00599.x 19220450

21. Hoffmann AA, Rieseberg LH (2008) Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Ann Rev Ecol Evol Syst 39 : 21–42.

22. Dobzhansky T (1937) Genetics and the origin of species. New York: Columbia University Press.

23. Muller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6 : 71–125.

24. Coyne JA, Orr HA (2004) Speciation. Sunderland, MA: Sinaeur Associates.

25. Fishman L, Willis JH (2001) Evidence for Dobzhansky-Muller incompatibilites contributing to the sterility of hybrids between Mimulus guttatus and M. nasutus. Evolution 55 : 1932–1942. 11761055

26. Sweigart AL, Fishman L, Willis JH (2006) A simple genetic incompatibility causes hybrid male sterility in Mimulus. Genetics 172 : 2465–2479. 16415357

27. Brideau NJ, Flores HA, Wang J, Maheshwari S, Wang X, et al. (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 : 1292–1295. 17124320

28. Meiklejohn CD, Holmbeck MA, Siddiq MA, Abt DN, Rand DM, et al. (2013) An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet 9.

29. Sawamura K, Yamamoto MT (1997) Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity 79 : 97–103.

30. Presgraves DC (2010) The molecular evolutionary basis of species formation. Nat Rev Genet 11 : 175–180. doi: 10.1038/nrg2718 20051985

31. Orr HA, Presgraves DC (2000) Speciation by postzygotic isolation: forces, genes and molecules. Bioessays 22 : 1085–1094. 11084624

32. Bank C, Buerger R, Hermisson J (2012) The limits to parapatric speciation: Dobzhansky-Muller incompatibilities in a continent-island model. Genetics 191 : 845–U345. doi: 10.1534/genetics.111.137513 22542972

33. Gavrilets S (1997) Single locus clines. Evolution 51 : 979–983.

34. Gompert Z, Parchman TL, Buerkle CA (2012) Genomics of isolation in hybrids. Philos T Roy Soc B 367 : 439–450.

35. Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, et al. (2014) Genomics and the origin of species. Nat Rev Genet 15 : 176–192. doi: 10.1038/nrg3644 24535286

36. Rieseberg LH, Blackman BK (2010) Speciation genes in plants. Ann Bot 106 : 439–455. doi: 10.1093/aob/mcq126 20576737

37. Johnson NA, Wolf JB, Brodie ED III, Wade MJ (2000) Gene interactions and the origin of species. In: Wolf J, Brodie EI, Wade M, editors. Epistasis and the evolutionary process. New York: Oxford University Press. pp. 197–212.

38. Gavrilets S (1997) Hybrid zones with Dobzhansky-type epistatic selection. Evolution 51 : 1027–1035.

39. Paixão T, Bassler KE, Azevedo RBR (2014) Emergent speciation by multiple Dobzhansky-Muller incompatibilities. bioRxiv doi: http://dx.doi.org/10.1101/008268.

40. Schartl M (2008) Evolution of Xmrk: an oncogene, but also a speciation gene? Bioessays 30 : 822–832. doi: 10.1002/bies.20807 18693261

41. Schumer M, Cui R, Powell D, Dresner R, Rosenthal G, et al. (2014) High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species. eLife 3: e02535.

42. Fang S, Yukilevich R, Chen Y, Turissini DA, Zeng K, et al. (2012) Incompatibility and competitive exclusion of genomic segments between sibling Drosophila species. PLoS Genet 8.

43. Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc London Ser B 273 : 1187–1193.

44. Hasselman DJ, Argo EE, McBride MC, Bentzen P, Schultz TF, et al. (2014) Human disturbance causes the formation of a hybrid swarm between two naturally sympatric fish species. Mol Ecol 23 : 1137–1152. doi: 10.1111/mec.12674 24450302

45. Rosenfield JA, Kodric-Brown A (2003) Sexual selection promotes hybridization between Pecos pupfish, Cyprinodon pecosensis and sheepshead minnow, C. variegatus. J Evolution Biol 16 : 595–606.

46. Karlin S (1975) General 2-locus selection models—Some objectives, results and interpretations. Theor Popul Biol 7 : 364–398. 1179266

47. Bodmer WF, Felsenstein J (1967) Linkage and selection—theoretical analysis of deterministic 2 locus random mating model. Genetics 57 : 237–265. 5584566

48. Gavrilets S (2004) Fitness landscapes and the origin of species. Princeton, NJ, USA: Princeton University Press. 1–432 p.

49. James JK, Abbott RJ (2005) Recent, allopatric, homoploid hybrid speciation: The origin of Senecio squalidus (Asteraceae) in the British Isles from a hybrid zone on Mount Etna, Sicily. Evolution 59 : 2533–2547. 16526502

50. Lexer C, Joseph JA, van Loo M, Barbara T, Heinze B, et al. (2010) Genomic Admixture Analysis in European Populus spp. Reveals Unexpected Patterns of Reproductive Isolation and Mating. Genetics 186 : 699–U391. doi: 10.1534/genetics.110.118828 20679517

51. Kunte K, Shea C, Aardema ML, Scriber JM, Juenger TE, et al. (2011) Sex Chromosome Mosaicism and Hybrid Speciation among Tiger Swallowtail Butterflies. PLoS Genetics 7 : 1–14.

52. Rubidge EM, Taylor EB (2004) Hybrid zone structure and the potential role of selection in hybridizing populations of native westslope cutthroat trout (Oncorhynchus clarki lewisi) and introduced rainbow trout (O. mykiss). Mol Ecol 13 : 3735–3749. 15548287

53. Trier CN, Hermansen JS, Sætre G-P, Bailey RI (2014) Evidence for mito-nuclear and sex-linked reproductive barriers between the hybrid Italian sparrow and its parent species. PLoS Genet 10.

54. Unckless RL, Orr HA (2009) Dobzhansky-Muller incompatibilities and adaptation to a shared environment. Heredity 102 : 214–217. doi: 10.1038/hdy.2008.129 19142201

55. Moyle LC, Graham EB (2006) Genome-wide associations between hybrid sterility QTL and marker transmission ratio distortion. Mol Biol Evol 23 : 973–980. 16495346

56. Masly JP, Presgraves DC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5 : 1890–1898.

57. Presgraves DC (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163 : 955–972. 12663535

58. Gardner K, Buerkle A, Whitton J, Rieseberg L (2000) Inferring epistasis in wild sunflower hybrid zones. In: Wolf JB, Brodie ED III, Wade MJ, editors. Epistasis and the evolutionary process. New York: Oxford University Press. pp. 264–279.

59. Payseur BA, Hoekstra HE (2005) Signatures of reproductive isolation in patterns of single nucleotide diversity across inbred strains of mice. Genetics 171 : 1905–1916. 16143616

60. Teeter KC, Payseur BA, Harris LW, Bakewell MA, Thibodeau LM, et al. (2008) Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res 18 : 67–76. 18025268

61. Ostberg CO, Slatton SL, Rodriguez RJ (2004) Spatial partitioning and asymmetric hybridization among sympatric coastal steelhead trout (Oncorhynchus mykiss irideus), coastal cutthroat trout (O. clarki clarki) and interspecific hybrids. Mol Ecol 13 : 2773–2788. 15315688

62. Field DL, Ayre DJ, Whelan RJ, Young AG (2011) Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida. Heredity 106 : 841–853. doi: 10.1038/hdy.2010.127 21063438

63. Greig D, Louis EJ, Borts RH, Travisano M (2002) Hybrid speciation in experimental populations of yeast. Science 298 : 1773–1775. 12459586

64. Buerkle CA, Rieseberg LH (2008) The rate of genome stabilization in homoploid hybrid species. Evolution 62 : 266–275. 18039323

65. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006) Homoploid hybrid speciation in an extreme habitat. Science 314 : 1923–1925. 17138866

66. Rieseberg LH, Whitton J, Gardner K (1999) Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. Genetics 152 : 713–727. 10353912

67. Servedio MR (2000) Reinforcement and the genetics of nonrandom mating. Evolution 54 : 21–29. 10937179

68. Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: Theory and data. Annu Rev Ecol Evol S 34 : 339–364.

69. Kirkpatrick M, Servedio MR (1999) The reinforcement of mating preferences on an island. Genetics 151 : 865–884. 9927476

70. Nosil P, Yukilevich R (2008) Mechanisms of reinforcement in natural and simulated polymorphic populations. Biol J Linnean Soc 95 : 305–319.

71. Rosenthal GG (2013) Individual mating decisions and hybridization. J Evol Biol 26 : 252–255. doi: 10.1111/jeb.12004 23323999

72. Fisher HS, Mascuch SJ, Rosenthal GG (2009) Multivariate male traits misalign with multivariate female preferences in the swordtail fish, Xiphophorus birchmanni. Anim Behav 78 : 265–269.

73. Culumber ZW, Ochoa OM, Rosenthal GG (2014) Assortative mating and the maintenance of population structure in a natural hybrid zone. Am Nat 184 : 225–232. doi: 10.1086/677033 25058282

74. Ganem G, Litel C, Lenormand T (2008) Variation in mate preference across a house mouse hybrid zone. Heredity 100 : 594–601. doi: 10.1038/hdy.2008.20 18414506

75. Matute DR, Butler IA, Turissini DA, Coyne JA (2010) A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329 : 1518–1521. doi: 10.1126/science.1193440 20847270

76. Corbett-Detig RB, Zhou J, Clark AG, Hartl DL, Ayroles JF (2013) Genetic incompatibilities are widespread within species. Nature 504 : 135–137. doi: 10.1038/nature12678 24196712

77. Harushima Y, Nakagahra M, Yano M, Sasaki T, Kurata N (2001) A genome-wide survey of reproductive barriers in an intraspecific hybrid. Genetics 159 : 883–892. 11606560

78. Janousek V, Wang L, Luzynski K, Dufkova P, Vyskocilova MM, et al. (2012) Genome-wide architecture of reproductive isolation in a naturally occurring hybrid zone between Mus musculus musculus and M. m. domesticus. Mol Ecol 21 : 3032–3047. doi: 10.1111/j.1365-294X.2012.05583.x 22582810

79. Turner LM, White MA, Tautz D, Payseur BA (2014) Genomic networks of hybrid sterility. PLoS Genet 10.

80. Gay L, Crochet P-A, Bell DA, Lenormand T (2008) Comparing clines on molecular and phenotypic traits in hybrid zones: A window on tension zone models. Evolution 62 : 2789–2806. doi: 10.1111/j.1558-5646.2008.00491.x 18752618

81. Nolte AW, Gompert Z, Buerkle CA (2009) Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Mol Ecol 18 : 2615–2627. doi: 10.1111/j.1365-294X.2009.04208.x 19457191

82. Vines TH, Kohler SC, Thiel A, Ghira I, Sands TR, et al. (2003) The maintenance of reproductive isolation in a mosaic hybrid zone between the fire-bellied toads Bombina bombina and B. variegata. Evolution 57 : 1876–1888. 14503629

83. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, et al. (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol 5 : 1962–1972.

84. Sweigart AL (2010) Simple Y-Autosomal incompatibilities cause hybrid male sterility in reciprocal crosses between Drosophila virilis and D. americana. Genetics 184 : 779–U225. doi: 10.1534/genetics.109.112896 20048051

85. Lee H-Y, Chou J-Y, Cheong L, Chang N-H, Yang S-Y, et al. (2008) Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135 : 1065–1073. doi: 10.1016/j.cell.2008.10.047 19070577

86. Rawson PD, Burton RS (2002) Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc Natl Acad Sci USA 99 : 12955–12958. 12271133

87. Johnson NA (2010) Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26 : 317–325. doi: 10.1016/j.tig.2010.04.005 20621759

88. Crespi B, Nosil P (2013) Conflictual speciation: species formation via genomic conflict. Trends Ecol Evol 28 : 48–57. doi: 10.1016/j.tree.2012.08.015 22995895

89. 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. 10747067

90. Maheshwari S, Barbash DA (2011) The genetics of hybrid incompatibilities. Ann Rev Genet 45 : 331–355. doi: 10.1146/annurev-genet-110410-132514 21910629

91. Staubach F, Lorenc A, Messer PW, Tang K, Petrov DA, et al. (2012) Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus). PLoS Genet 8.

92. Pritchard VL, Edmands S (2013) The genomic trajectory of hybrid swarms: outcomes of repeated crosses between populations of Tigriopus californicus. Evolution 67 : 774–791. doi: 10.1111/j.1558-5646.2012.01814.x 23461327

93. Schwander T, Suni SS, Cahan SH, Keller L (2008) Mechanisms of reproductive isolation between an ant species of hybrid origin and one of its parents. Evolution 62 : 1635–1643. doi: 10.1111/j.1558-5646.2008.00387.x 18373626

94. Hermansen JS, Haas F, Trier CN, Bailey RI, Nederbragt AJ, et al. (2014) Hybrid speciation through sorting of parental incompatibilities in Italian sparrows. Mol Ecol doi: 10.1111/mec.12910

95. Gross BL, Rieseberg LH (2005) The ecological genetics of homoploid hybrid speciation. J Hered 96 : 241–252. 15618301

96. Hastings A (1984) Linkage disequilibrium, selection and recombination at three loci. Genetics 106 : 153–164. 17246189

97. Kirkpatrick M, Johnson T, Barton N (2002) General models of multilocus evolution. Genetics 161 : 1727–1750. 12196414

98. Gardner A, West SA, Barton NH (2007) The relation between multilocus population genetics and social Evolution Theory. Am Nat 169 : 207–226. 17211805

99. Kopp M, Gavrilets S (2006) Multilocus genetics and the coevolution of quantitative traits. Evolution 60 : 1321–1336. 16929650