Genetic conflicts: The usual suspects and beyond

Journal of Experimental Biology

Volumn 220, Issue 1, 2017, Pages 6-17

  McLaughlin, Richard N ^a   Malik, Harmit S ^a,b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Antagonism; Host pathogen; Meiosis; Mitochondria; Mutualism; Red Queen; Toxin antitoxin; Wolbachia

Indexed keywords

TRANSPOSON;

ADAPTATION; ANIMAL; BIOLOGICAL MODEL; EVOLUTION; GENETIC SELECTION; GENOME; GENOTYPE ENVIRONMENT INTERACTION; HOST PATHOGEN INTERACTION; HUMAN; MEIOSIS; MOLECULAR EVOLUTION; TRANSPOSON;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENE-ENVIRONMENT INTERACTION; GENOME; HOST-PATHOGEN INTERACTIONS; HUMANS; MEIOSIS; MODELS, GENETIC; SELECTION, GENETIC;

EID: 85010408044     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.148148     Document Type: Review

References (169)

1. Adachi-Hagimori, T., Miura, K. and Stouthamer, R. (2008). A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. Proc. R. Soc. B Biol. Sci. 275, 2667-2673.
2. Aebischer, T.,Moskophidis, D.,Rohrer, U.H., Zinkernagel, R.M. and Hengartner, H. (1991). In vitro selection of lymphocytic choriomeningitis virus escape mutants by cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 88, 11047-11051.
3. Agrawal, A., Eastman, Q. M. and Schatz, D. G. (1998). Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394, 744-751.
4. Arnegard, M. E., McGee, M. D., Matthews, B., Marchinko, K. B., Conte, G. L., Kabir, S., Bedford, N., Bergek, S., Chan, Y. F., Jones, F. C. et al. (2014). Genetics of ecological divergence during speciation. Nature 511, 307-311.
5. Barbash, D. A., Siino, D. F., Tarone, A. M. and Roote, J. (2003). A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl. Acad. Sci. USA 100, 5302-5307.
6. Barr, C. M. and Fishman, L. (2010). The nuclear component of a cytonuclear hybrid incompatibility in Mimulus maps to a cluster of pentatricopeptide repeat genes. Genetics 184, 455-465.
7. Barrick, J. E. and Lenski, R. E. (2013). Genome dynamics during experimental evolution. Nat. Rev. Genet. 14, 827-839.
8. Beck, C. R., Garcia-Perez, J. L., Badge, R. M. and Moran, J. V. (2011). LINE-1 elements in structural variation and disease. Annu. Rev. Genomics Hum. Genet. 12, 187-215.
9. Beeman, R. W., Friesen, K. S. and Denell, R. E. (1992). Maternal-effect selfish genes in flour beetles. Science 256, 89-92.
10. Benit, L., De Parseval, N., Casella, J. F., Callebaut, I., Cordonnier, A. and Heidmann, T. (1997). Cloning of a new murine endogenous retrovirus, MuERV-L, with strong similarity to the human HERV-L element and with a gag coding sequence closely related to the Fv1 restriction gene. J. Virol. 71, 5652-5657.
11. Bergthorsson, U., Andersson, D. I. and Roth, J. R. (2007). Ohno's dilemma: Evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. USA 104, 17004-17009.
12. Best, S., Le Tissier, P., Towers, G. and Stoye, J. P. (1996). Positional cloning of the mouse retrovirus restriction gene Fv1. Nature 382, 826-829.
13. Bestor, T. H. (2003). Cytosine methylation mediates sexual conflict. Trends Genet. 19, 185-190.
14. Boissinot, S., Entezam, A. and Furano, A. V. (2001). Selection against deleterious LINE-1-containing loci in the human lineage. Mol. Biol. Evol. 18, 926-935.
15. Bordenstein, S. R. andWerren, J. H. (1998). Effects of A and BWolbachia and host genotype on interspecies cytoplasmic incompatibility in Nasonia. Genetics 148, 1833-1844.
16. Bourc'his, D. and Bestor, T. H. (2004). Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99.
17. Brennan, G., Kitzman, J. O., Rothenburg, S., Shendure, J. and Geballe, A. P. (2014). Adaptive gene amplification as an intermediate step in the expansion of virus host range. PLoS Pathog. 10, e1004002.
18. Brideau, N. J., Flores, H. A., Wang, J., Maheshwari, S., Wang, X. and Barbash, D. A. (2006). Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314, 1292-1295.
19. Brouha, B., Schustak, J., Badge, R. M., Lutz-Prigge, S., Farley, A. H., Moran, J. V. and Kazazian, H. H., Jr. (2003). Hot L1s account for the bulk of retrotransposition in the human population. Proc. Natl. Acad. Sci. USA 100, 5280-5285.
20. Buckler, E. S. t., Phelps-Durr, T. L., Buckler, C. S., Dawe, R. K., Doebley, J. F. and Holtsford, T. P. (1999). Meiotic drive of chromosomal knobs reshaped the maize genome. Genetics 153, 415-426.
21. Budar, F., Touzet, P. and De Paepe, R. (2003). The nucleo-mitochondrial conflict in cytoplasmic male sterilities revisited. Genetica 117, 3-16.
22. Burt, A. and Trivers, R. (2006). Genes in Conflict: The Biology of Selfish Genetic Elements. Cambridge, Mass: Belknap Press of Harvard University Press.
23. Camus, M. F., Wolf, J. B. W., Morrow, E. H. and Dowling, D. K. (2015). Single nucleotides in the mtDNA sequence modify mitochondrial molecular function and are associated with sex-specific effects on fertility and aging. Curr. Biol. 25, 2717-2722.
24. Cantrell, M. A., Scott, L., Brown, C. J., Martinez, A. R. and Wichman, H. A. (2008). Loss of LINE-1 activity in the megabats. Genetics 178, 393-404.
25. Carroll, S. B. (2000). Endless forms: The evolution of gene regulation and morphological diversity. Cell 101, 577-580.
26. Carroll, L. and Tenniel, J. (1871). Through the Looking-Glass, and What Alice Found There. New York: Macmillan.
27. Case, A. L. and Willis, J. H. (2008). Hybrid male sterility in Mimulus (Phrymaceae) is associated with a geographically restricted mitochondrial rearrangement. Evolution 62, 1026-1039.
28. Castro-Diaz, N., Ecco, G., Coluccio, A., Kapopoulou, A., Yazdanpanah, B., Friedli, M., Duc, J., Jang, S. M., Turelli, P. and Trono, D. (2014). Evolutionally dynamic L1 regulation in embryonic stem cells. Genes Dev. 28, 1397-1409.
29. Chase, C. D. (2007). Cytoplasmic male sterility: A window to the world of plant mitochondrial-nuclear interactions. Trends Genet. 23, 81-90.
30. Chmátal, L., Gabriel, S. I., Mitsainas, G. P., Martínez-Vargas, J., Ventura, J., Searle, J. B., Schultz, R. M. and Lampson, M. A. (2014). Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr. Biol. 24, 2295-2300.
31. Chuong, E. B., Elde, N. C. and Feschotte, C. (2016). Regulatory evolution of innate immunity through co-option of endogenous retroviruses. Science 351, 1083-1087.
32. Ciurea, A., Klenerman, P., Hunziker, L., Horvath, E., Senn, B. M., Ochsenbein, A. F., Hengartner, H. and Zinkernagel, R. M. (2000). Viral persistence in vivo through selection of neutralizing antibody-escape variants. Proc. Natl. Acad. Sci. USA 97, 2749-2754.
33. Clarke, B. (1962). Balanced polymorphism and the diversity of sympatric species. In Taxonomy and Geography (ed. D. Nichols), pp. 47-70. Oxford: Systematics Association.
34. Compton, A. A., Malik, H. S. and Emerman, M. (2013). Host gene evolution traces the evolutionary history of ancient primate lentiviruses. Philos. Trans. R. Soc. B Biol. Sci. 368, 20120496.
35. Crotty, S., Cameron, C. E. and Andino, R. (2001). RNA virus error catastrophe: Direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. USA 98, 6895-6900.
36. Daugherty, M. D. and Malik, H. S. (2012). Rules of engagement: Molecular insights from host-virus arms races. Annu. Rev. Genet. 46, 677-700.
37. Dawe, R. K. and Cande, W. Z. (1996). Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc. Natl. Acad. Sci. USA 93, 8512-8517.
38. Dawkins, R. (1976). The Selfish Gene. Oxford: Oxford University Press.
39. de Koning, A. P. J., Gu, W., Castoe, T. A., Batzer, M. A. and Pollock, D. D. (2011). Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 7, e1002384.
40. Demuth, J. P. and Hahn, M. W. (2009). The life and death of gene families. Bioessays 31, 29-39.
41. Domingo, E., Sheldon, J. and Perales, C. (2012). Viral quasispecies evolution. Microbiol. Mol. Biol. Rev. 76, 159-216.
42. Doolittle, W. F. and Sapienza, C. (1980). Selfish genes, the phenotype paradigm and genome evolution. Nature 284, 601-603.
43. Drake, J. W. (1999). The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Ann. N. Y. Acad. Sci. 870, 100-107.
44. Dunham, M. J., Badrane, H., Ferea, T., Adams, J., Brown, P. O., Rosenzweig, F. and Botstein, D. (2002). Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99, 16144-16149.
45. Dupressoir, A., Lavialle, C. and Heidmann, T. (2012). From ancestral infectious retroviruses to bona fide cellular genes: Role of the captured syncytins in placentation. Placenta 33, 663-671.
46. Eigen, M. and Schuster, P. (1977). A principle of natural self-organization. Part A: Emergence of the hypercycle. Naturwissenschaften 64, 541-565.
47. Eldar, A. (2011). Social conflict drives the evolutionary divergence of quorum sensing. Proc. Natl. Acad. Sci. USA 108, 13635-13640.
48. Elde, N. C., Child, S. J., Geballe, A. P. and Malik, H. S. (2009). Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457, 485-489.
49. Elde, N. C., Child, S. J., Eickbush, M. T., Kitzman, J. O., Rogers, K. S., Shendure, J., Geballe, A. P. and Malik, H. S. (2012). Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses. Cell 150, 831-841.
50. Emerman, M. and Malik, H. S. (2010). Paleovirology-modern consequences of ancient viruses. PLoS Biol. 8, e1000301.
51. Feschotte, C. (2008). Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9, 397-405.
52. Fischer, S., Zottl, M., Groenewoud, F. and Taborsky, B. (2014). Group-sizedependent punishment of idle subordinates in a cooperative breeder where helpers pay to stay. Proc. R. Soc. B Biol. Sci. 281, 20140184.
53. Fishman, L. and Kelly, J. K. (2015). Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution 69, 1208-1218.
54. Fishman, L. and Saunders, A. (2008). Centromere-associated female meiotic drive entails male fitness costs in monkeyflowers. Science 322, 1559-1562.
55. Foster, K. R. and Ratnieks, F. L.W. (2001). Convergent evolution of worker policing by egg eating in the honeybee and common wasp. Proc. R. Soc. B Biol. Sci. 268, 169-174.
56. Frank, S. A. (1991). Divergence of meiotic drive-suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45, 262-267.
57. Friberg, U. and Rice, W. R. (2015). Sexually antagonistic zygotic drive: A new form of genetic conflict between the sex chromosomes. Cold Spring Harb. Perspect. Biol. 7, a017608.
58. Friberg, U., Stewart, A. D. and Rice, W. R. (2011). Empirical evidence for sonkilling X chromosomes and the operation of SA-zygotic drive. PLoS ONE 6, e23508.
59. Frost, J. M. and Moore, G. E. (2010). The importance of imprinting in the human placenta. PLoS Genet. 6, e1001015.
60. Fujii, S., Bond, C. S. and Small, I. D. (2011). Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution. Proc. Natl. Acad. Sci. USA 108, 1723-1728.
61. Fukui, T., Kawamoto, M., Shoji, K., Kiuchi, T., Sugano, S., Shimada, T., Suzuki, Y. and Katsuma, S. (2015). The endosymbiotic bacterium Wolbachia selectively kills male hosts by targeting the masculinizing gene. PLoS Pathog. 11, e1005048.
62. Goodier, J. L., Pereira, G., Cheung, L. E., Rose, R. and Kazazian, H. H., Jr. (2015). The broad-spectrum antiviral protein ZAP restricts human retrotransposition. PLoS Genet. 11, e1005252.
63. Grahn, R. A., Rinehart, T. A., Cantrell, M. A. and Wichman, H. A. (2005). Extinction of LINE-1 activity coincident with a major mammalian radiation in rodents. Cytogenet. Genome Res. 110, 407-415.
64. Haig, D. (2004). Genomic imprinting and kinship: How good is the evidence? Annu. Rev. Genet. 38, 553-585.
65. Haig, D. (2014). Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting. Heredity 113, 96-103.
66. Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos 35, 282-290.
67. Hammond, T. M., Rehard, D. G., Xiao, H. and Shiu, P. K. (2012). Molecular dissection of Neurospora Spore killer meiotic drive elements. Proc. Natl. Acad. Sci. USA 109, 12093-12098.
68. Hartl, D. L. (1975). Modifier theory and meiotic drive. Theor. Popul. Biol. 7, 168-174.
69. Hauser, M. D. (1992). Costs of deception: Cheaters are punished in rhesus monkeys (Macaca mulatta). Proc. Natl. Acad. Sci. USA 89, 12137-12139.
70. Henikoff, S., Ahmad, K. and Malik, H. S. (2001). The centromere paradox: Stable inheritance with rapidly evolving DNA. Science 293, 1098-1102.
71. Hiom, K., Melek, M. and Gellert, M. (1998). DNA transposition by the RAG1 and RAG2 proteins: A possible source of oncogenic translocations. Cell 94, 463-470.
72. Holmes, E. C. (2008). Evolutionary history and phylogeography of human viruses. Annu. Rev. Microbiol. 62, 307-328.
73. Hu, S., Li, J., Xu, F., Mei, S., Le Duff, Y., Yin, L., Pang, X., Cen, S., Jin, Q., Liang, C. et al. (2015). SAMHD1 inhibits LINE-1 retrotransposition by promoting stress granule formation. PLoS Genet. 11, e1005367.
74. Hurst, G. D. and Jiggins, F. M. (2000). Male-killing bacteria in insects: Mechanisms, incidence, and implications. Emerg. Infect. Dis. 6, 329-336.
75. Hurst, L. D. and Pomiankowski, A. (1991). Causes of sex ratio bias may account for unisexual sterility in hybrids: A new explanation of Haldane's rule and related phenomena. Genetics 128, 841-858.
76. Hurst, G. D. D. and Werren, J. H. (2001). The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2, 597-606.
77. Hurst, L. D., Atlan, A. and Bengtsson, B. O. (1996). Genetic conflicts. Q. Rev. Biol. 71, 317-364.
78. Jacobs, F. M. J., Greenberg, D., Nguyen, N., Haeussler, M., Ewing, A. D., Katzman, S., Paten, B., Salama, S. R. and Haussler, D. (2014). An evolutionary arms race between KRAB zinc-finger genes ZNF91/93 and SVA/L1 retrotransposons. Nature 516, 242-245.
79. Johnson, N. A. (2010). Hybrid incompatibility genes: Remnants of a genomic battlefield? Trends Genet. 26, 317-325.
80. Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O. and Walichiewicz, J. (2005). Repbase Update, a database of eukaryotic repetitive elements. Cytogenet. Genome Res. 110, 462-467.
81. Kageyama, D., Nishimura, G., Hoshizaki, S. and Ishikawa, Y. (2002). Feminizing Wolbachia in an insect, Ostrinia furnacalis (Lepidoptera: Crambidae). Heredity 88, 444-449.
82. Kobayashi, I. (1996). DNA Modification and Restriction: Selfish Behavior of an Epigenetic System. Cold Spring Harbor Monograph Archive.
83. Kobayashi, I. (2001). Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 29, 3742-3756.
84. Koonin, E. V. and Starokadomskyy, P. (2016). Are viruses alive? The replicator paradigm sheds decisive light on an old but misguided question. Stud. Hist. Philos. Biol. Biomed. Sci. 59, 125-134.
85. Kugelberg, E., Kofoid, E., Andersson, D. I., Lu, Y., Mellor, J., Roth, F. P. and Roth, J. R. (2010). The tandem inversion duplication in Salmonella enterica: Selection drives unstable precursors to final mutation types. Genetics 185, 65-80.
86. Kunarso, G., Chia, N.-Y., Jeyakani, J., Hwang, C., Lu, X., Chan, Y.-S., Ng, H.-H. and Bourque, G. (2010). Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat. Genet. 42, 631-634.
87. Kusano, A., Staber, C., Chan, H. Y. E. and Ganetzky, B. (2003). Closing the (Ran) GAP on segregation distortion in Drosophila. Bioessays 25, 108-115.
88. Lander, E. S. Linton, L. M. Birren, B. Nusbaum, C. Zody, M. C. Baldwin, J. Devon, K. Dewar, K. Doyle, M. FitzHugh, W. et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921.
89. Laurie, C. C. (1997). The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics 147, 937-951.
90. Leppä lä , J. and Savolainen, O. (2011). Nuclear-cytoplasmic interactions reduce male fertility in hybrids of Arabidopsis lyrata subspecies. Evolution 65, 2959-2972.
91. Lim, E. S., Fregoso, O. I., McCoy, C. O., Matsen, F. A., Malik, H. S. and Emerman, M. (2012). The ability of primate lentiviruses to degrade the monocyte restriction factor SAMHD1 preceded the birth of the viral accessory protein Vpx. Cell Host Microbe 11, 194-204.
92. Lindholm, A. K., Dyer, K. A., Firman, R. C., Fishman, L., Forstmeier, W., Holman, L., Johannesson, H., Knief, U., Kokko, H., Larracuente, A. M. et al. (2016). The ecology and evolutionary dynamics of meiotic drive. Trends Ecol. Evol. 31, 315-326.
93. Lorenzen, M. D., Gnirke, A., Margolis, J., Garnes, J., Campbell, M., Stuart, J. J., Aggarwal, R., Richards, S., Park, Y. and Beeman, R. W. (2008). The maternaleffect, selfish genetic element Medea is associated with a composite Tc1 transposon. Proc. Natl. Acad. Sci. USA 105, 10085-10089.
94. Lynch, V. J. (2016). GENETICS. A copy-and-paste gene regulatory network. Science 351, 1029-1030.
95. Maheshwari, S. and Barbash, D. A. (2011). The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45, 331-355.
96. Malki, S., van der Heijden, G. W., O'Donnell, K. A., Martin, S. L. and Bortvin, A. (2014). A role for retrotransposon LINE-1 in fetal oocyte attrition in mice. Dev. Cell 29, 521-533.
97. Mason, J. M. and Biessmann, H. (1995). The unusual telomeres of Drosophila. Trends Genet. 11, 58-62.
98. McLaughlin, R. N., Jr., Young, J. M., Yang, L., Neme, R., Wichman, H. A. and Malik, H. S. (2014). Positive selection and multiple losses of the LINE-1-derived L1TD1 gene in mammals suggest a dual role in genome defense and pluripotency. PLoS Genet. 10, e1004531.
99. Melnick, J. L., Crowther, D. and Barrera-Oro, J. (1961). Rapid development of drug-resistant mutants of poliovirus. Science 134, 557.
100. Messer, P.W. and Petrov, D. A. (2013). Population genomics of rapid adaptation by soft selective sweeps. Trends Ecol. Evol. 28, 659-669.
101. Meyerson, N. R. and Sawyer, S. L. (2011). Two-stepping through time: Mammals and viruses. Trends Microbiol. 19, 286-294.
102. Mitchell, P. S., Patzina, C., Emerman, M., Haller, O., Malik, H. S. and Kochs, G. (2012). Evolution-guided identification of antiviral specificity determinants in the broadly acting interferon-induced innate immunity factor MxA. Cell Host Microbe 12, 598-604.
103. Molaro, A. and Malik, H. S. (2016). Hide and seek: How chromatin-based pathways silence retroelements in the mammalian germline. Curr. Opin. Genet. Dev. 37, 51-58.
104. Moldovan, J. B. and Moran, J. V. (2015). The zinc-finger antiviral protein ZAP inhibits LINE and Alu Retrotransposition. PLoS Genet. 11, e1005121.
105. Montgomery, E., Charlesworth, B. and Langley, C. H. (2007). A test for the role of natural selection in the stabilization of transposable element copy number in a population of Drosophila melanogaster. Genet. Res. 89, 435-445.
106. Moran, N. A., McCutcheon, J. P. and Nakabachi, A. (2008). Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165-190.
107. Muckenfuss, H., Hamdorf, M., Held, U., Perković, M., Löwer, J., Cichutek, K., Flory, E., Schumann, G. G. and Munk, C. (2006). APOBEC3 proteins inhibit human LINE-1 retrotransposition. J. Biol. Chem. 281, 22161-22172.
108. Nair, S., Miller, B., Barends, M., Jaidee, A., Patel, J., Mayxay, M., Newton, P., Nosten, F., Ferdig, M. T. and Anderson, T. J. (2008). Adaptive copy number evolution in malaria parasites. PLoS Genet. 4, e1000243.
109. Najafabadi, H. S., Mnaimneh, S., Schmitges, F.W., Garton, M., Lam, K. N., Yang, A., Albu, M., Weirauch, M. T., Radovani, E., Kim, P. M. et al. (2015). C2H2 zinc finger proteins greatly expand the human regulatory lexicon. Nat. Biotechnol. 33, 555-562.
110. Nowak, M. A. (2006). Five rules for the evolution of cooperation. Science 314, 1560-1563.
111. Orgel, L. E. and Crick, F. H. C. (1980). Selfish DNA: The ultimate parasite. Nature 284, 604-607.
112. Orgel, L. E., Crick, F. H. C. and Sapienza, C. (1980). Selfish DNA. Nature 288, 645-646.
113. Patel, M. R., Emerman, M. and Malik, H. S. (2011). Paleovirology-ghosts and gifts of viruses past. Curr. Opin. Virol. 1, 304-309.
114. Patel, M. R., Loo, Y.-M., Horner, S. M., Gale, M., Jr. and Malik, H. S. (2012). Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biol. 10, e1001282.
115. Patel, M. R., Miriyala, G. K., Littleton, A. J., Yang, H., Trinh, K., Young, J. M., Kennedy, S. R., Yamashita, Y. M., Pallanck, L. J. and Malik, H. S. (2016). A mitochondrial DNA hypomorph of cytochrome oxidase specifically impairs male fertility in Drosophila melanogaster. eLife 5, 1144.
116. Peacock, W. J., Dennis, E. S., Rhoades, M. M. and Pryor, A. J. (1981). Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc. Natl. Acad. Sci. USA 78, 4490-4494.
117. Pfennig, D.W., Harcombe, W. R. and Pfennig, K. S. (2001). Frequency-dependent Batesian mimicry. Nature 410, 323.
118. Phadnis, N. and Orr, H. A. (2009). A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376-379.
119. Prä nting, M. and Andersson, D. I. (2011). Escape from growth restriction in small colony variants of Salmonella typhimurium by gene amplification and mutation. Mol. Microbiol. 79, 305-315.
120. Prasad, N. G., Bedhomme, S., Day, T. and Chippindale, A. K. (2007). An evolutionary cost of separate genders revealed by male-limited evolution. Am. Nat. 169, 29-37.
121. Presgraves, D. C. (2010). The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11, 175-180.
122. Raju, N. B. (1994). Ascomycete spore killers: Chromosomal elements that distort genetic ratios among the products of meiosis. Mycologia 86, 461-473.
123. Rhoades, M. M. (1942). Preferential segregation in maize. Genetics 27, 395-407.
124. Rice, W. R. (1998). Male fitness increases when females are eliminated from gene pool: Implications for the Y chromosome. Proc. Natl. Acad. Sci. USA 95, 6217-6221.
125. Rice, R. W. and Holland, B. (1997). The enemies within: Intergenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behav. Ecol. Sociobiol. 41, 1-10.
126. Rice, W. R., Gavrilets, S. and Friberg, U. (2008). Sexually antagonistic "zygotic drive" of the sex chromosomes. PLoS Genet. 4, e1000313.
127. Rieseberg, L. H. and Blackman, B. K. (2010). Speciation genes in plants. Ann. Bot. 106, 439-455.
128. Ross, B. D. and Malik, H. S. (2014). Genetic conflicts: Stronger centromeres win tug-of-war in female meiosis. Curr. Biol. 24, R966-R968.
129. Sawyer, S. L., Wu, L. I., Emerman, M. and Malik, H. S. (2005). Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc. Natl. Acad. Sci. USA 102, 2832-2837.
130. Schnable, P. S. and Wise, R. P. (1998). The molecular basis of cytoplasmic male sterility. Trends Plant Sci. 3, 175-180.
131. Schnable, P. S.Ware, D. Fulton, R. S. Stein, J. C.Wei, F. Pasternak, S. Liang, C. Zhang, J. Fulton, L. Graves, T. A. et al. (2009). The B73 maize genome: Complexity, diversity, and dynamics. Science 326, 1112-1115.
132. Seidel, H. S., Ailion, M., Li, J., van Oudenaarden, A., Rockman, M. V. and Kruglyak, L. (2011). A novel sperm-delivered toxin causes late-stage embryo lethality and transmission ratio distortion in C. elegans. PLoS Biol. 9, e1001115.
133. Sheen, F. M. and Levis, R. W. (1994). Transposition of the LINE-like retrotransposon TART to Drosophila chromosome termini. Proc. Natl. Acad. Sci. USA 91, 12510-12514.
134. Simon, M., Durand, S., Pluta, N., Gobron, N., Botran, L., Ricou, A., Camilleri, C. and Budar, F. (2016). Genomic Conflicts that cause pollen mortality and raise reproductive barriers in Arabidopsis thaliana. Genetics 203, 1353-1367.
135. Singer, M. J., Mesner, L. D., Friedman, C. L., Trask, B. J. and Hamlin, J. L. (2000). Amplification of the human dihydrofolate reductase gene via double minutes is initiated by chromosome breaks. Proc. Natl. Acad. Sci. USA 97, 7921-7926.
136. Smit, A. F. and Riggs, A. D. (1996). Tiggers and DNA transposon fossils in the human genome. Proc. Natl. Acad. Sci. USA 93, 1443-1448
137. Song, M. and Boissinot, S. (2007). Selection against LINE-1 retrotransposons results principally from their ability to mediate ectopic recombination. Gene 390, 206-213.
138. Stambuk, B. U., Dunn, B., Alves, S. L., Jr., Duval, E. H. and Sherlock, G. (2009). Industrial fuel ethanol yeasts contain adaptive copy number changes in genes involved in vitamin B1 and B6 biosynthesis. Genome Res. 19, 2271-2278.
139. Stremlau, M., Owens, C. M., Perron, M. J., Kiessling, M., Autissier, P. and Sodroski, J. (2004). The cytoplasmic body component TRIM5alpha restricts HIV- 1 infection in Old World monkeys. Nature 427, 848-853.
140. Stremlau, M., Perron, M., Welikala, S. and Sodroski, J. (2005). Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J. Virol. 79, 3139-3145.
141. Sun, S., Berg, O. G., Roth, J. R. and Andersson, D. I. (2009). Contribution of gene amplification to evolution of increased antibiotic resistance in Salmonella typhimurium. Genetics 182, 1183-1195.
142. Swanson, W. J. and Vacquier, V. D. (2002). The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137-144.
143. Takahashi, N., Naito, Y., Handa, N. and Kobayashi, I. (2002). A DNA methyltransferase can protect the genome from postdisturbance attack by a restriction-modification gene complex. J. Bacteriol. 184, 6100-6108.
144. Tao, Y., Hartl, D. L. and Laurie, C. C. (2001). Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc. Natl. Acad. Sci. USA 98, 13183-13188.
145. Tao, Y., Araripe, L., Kingan, S. B., Ke, Y., Xiao, H. and Hartl, D. L. (2007a). A sexratio meiotic drive system in Drosophila simulans. II: An X-linked distorter. PLoS Biol. 5, e293.
146. Tao, Y., Masly, J. P., Araripe, L., Ke, Y. and Hartl, D. L. (2007b). A sex-ratio meiotic drive system in Drosophila simulans. I: An autosomal suppressor. PLoS Biol. 5, e292.
147. Tenaillon, O., Barrick, J. E., Ribeck, N., Deatherage, D. E., Blanchard, J. L., Dasgupta, A., Wu, G. C.,Wielgoss, S., Cruveiller, S., Medigue, C. et al. (2016). Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536, 165-170.
148. Thomas, J. H. and Schneider, S. (2011). Coevolution of retroelements and tandem zinc finger genes. Genome Res. 21, 1800-1812.
149. Thomson, M. S. and Beeman, R. W. (1999). Assisted suicide of a selfish gene. J. Hered. 90, 191-194.
150. Tudor, M., Lobocka, M., Goodell, M., Pettitt, J. and O'Hare, K. (1992). The pogo transposable element family of Drosophila melanogaster. Mol. Gen. Genet. 232, 126-134.
151. Turelli, P., Castro-Diaz, N., Marzetta, F., Kapopoulou, A., Raclot, C., Duc, J., Tieng, V., Quenneville, S. and Trono, D. (2014). Interplay of TRIM28 and DNA methylation in controlling human endogenous retroelements. Genome Res. 24, 1260-1270.
152. Unterholzner, S. J., Poppenberger, B. and Rozhon, W. (2014). Toxin-antitoxin systems: Biology, identification, and application. Mob. Genet. Elements 3, e26219.
153. Vacquier, V. D. and Swanson, W. J. (2011). Selection in the rapid evolution of gamete recognition proteins in marine invertebrates. Cold Spring Harb. Perspect. Biol. 3, a002931.
154. Van Valen, L. (1973). A new evolutionary law. Evol. Theory 1, 1-30.
155. Vaquerizas, J. M., Kummerfeld, S. K., Teichmann, S. A. and Luscombe, N. M. (2009). A census of human transcription factors: Function, expression and evolution. Nat. Rev. Genet. 10, 252-263.
156. Vignuzzi, M., Stone, J. K., Arnold, J. J., Cameron, C. E. and Andino, R. (2006). Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439, 344-348.
157. Wang, Z., Zou, Y., Li, X., Zhang, Q., Chen, L., Wu, H., Su, D., Chen, Y., Guo, J., Luo, D. et al. (2006). Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18, 676-687.
158. Wang, T., Zeng, J., Lowe, C. B., Sellers, R. G., Salama, S. R., Yang, M., Burgess, S. M., Brachmann, R. K. and Haussler, D. (2007). Species-specific endogenous retroviruses shape the transcriptional network of the human tumor suppressor protein p53. Proc. Natl. Acad. Sci. USA 104, 18613-18618.
159. Weeks, A. R., Turelli, M., Harcombe, W. R., Reynolds, K. T. and Hoffmann, A. A. (2007). From parasite to mutualist: Rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5, e114.
160. Weirauch, M. T. and Hughes, T. R. (2011). A catalogue of eukaryotic transcription factor types, their evolutionary origin, and species distribution. Subcell. Biochem. 52, 25-73.
161. Werren, J. H. (2011). Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl. Acad. Sci. USA 108 Suppl. 2, 10863-10870.
162. Wertheim, J. O. and Worobey, M. (2009). Dating the age of the SIV lineages that gave rise to HIV-1 and HIV-2. PLoS Comput. Biol. 5, e1000377.
163. Wolf, D. and Goff, S. P. (2009). Embryonic stem cells use ZFP809 to silence retroviral DNAs. Nature 458, 1201-1204.
164. Wolf, J. B. and Hager, R. (2006). A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol. 4, e380.
165. Wu, C.-I., Lyttle, T. W., Wu, M.-L. and Lin, G.-F. (1988). Association between a satellite DNA sequence and the Responder of Segregation Distorter in D. melanogaster. Cell 54, 179-189.
166. Yan, Y., Buckler-White, A., Wollenberg, K. and Kozak, C. A. (2009). Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. Proc. Natl. Acad. Sci. USA 106, 3259-3263.
167. Yang, Z. and Bielawski, J. P. (2000). Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496-503.
168. Yap, M. W., Nisole, S. and Stoye, J. P. (2005). A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr. Biol. 15, 73-78.
169. Zanders, S. E., Eickbush, M. T., Yu, J. S., Kang, J.-W., Fowler, K. R., Smith, G. R. and Malik, H. S. (2014). Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. eLife 3, e02630.