Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Schumer, Molly ^a   Cui, Rongfeng ^b,c,d   Rosenthal, Gil G ^b,c   Andolfatto, Peter ^a  

^a PRINCETON UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Centro de Investigaciones Científicas de las Huastecas Colonia Aguazarca   (Mexico)

^d MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; ASSORTATIVE MATING; CALCULATION; CONTROLLED STUDY; GENETIC INCOMPATIBILITY; GENOTYPE; HUMAN; HYBRID; IMMIGRATION; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; POPULATION MIGRATION; PREDICTION; REPRODUCTIVE FITNESS; REPRODUCTIVE ISOLATION; SEXUAL SELECTION; SIMULATION; BIOLOGICAL MODEL; GENE FLOW; GENETIC DRIFT; GENETIC SELECTION; GENETIC VARIATION; HYBRIDIZATION; POPULATION GENETICS; SPECIES DIFFERENTIATION; THEORETICAL MODEL;

GENE FLOW; GENETIC DRIFT; GENETIC SPECIATION; GENETIC VARIATION; GENETICS, POPULATION; HYBRIDIZATION, GENETIC; MODELS, GENETIC; MODELS, THEORETICAL; REPRODUCTIVE ISOLATION; SELECTION, GENETIC;

EID: 84926200660     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005041     Document Type: Article

References (99)

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, Brigham CA, Schwarz MW, (2003) The origin and extinction of species through hybridization. In: 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, IIIWade MJ, Wolf J, Brodie EI, Wade M, (2000) Gene interactions and the origin of species. In: 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, Wolf JB, Brodie ED, IIIWade MJ, (2000) Inferring epistasis in wild sunflower hybrid zones. In: 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