Introgression in the Drosophila subobscura-D. madeirensis sister species: Evidence of gene flow in nuclear genes despite mitochondrial differentiation

Evolution

Volumn 68, Issue 3, 2014, Pages 705-719

  Herrig, Danielle K ^a   Modrick, Alec J ^a   Brud, Evgeny ^a   Llopart, Ana ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Adaptation; Gene flow; Inversions; Population genetics; Speciation

Indexed keywords

CHROMOSOME; DIVERGENCE; FLY; GENE EXPRESSION; GENE FLOW; GENETIC DIFFERENTIATION; INTROGRESSION; MITOCHONDRIAL DNA; POLYMORPHISM; SPECIATION (BIOLOGY); STERILITY;

DROSOPHILA GUANCHE; DROSOPHILA MADEIRENSIS; DROSOPHILA SUBOBSCURA;

ADAPTATION; ANIMAL; ARTICLE; DROSOPHILA; GENE; GENE FLOW; GENETIC POLYMORPHISM; GENETICS; INSECT CHROMOSOME; INVERSIONS; MITOCHONDRIAL GENE; POPULATION GENETICS; SPECIES DIFFERENTIATION; Y CHROMOSOME;

ADAPTATION; GENE FLOW; INVERSIONS; POPULATION GENETICS; SPECIATION;

ANIMALS; CHROMOSOMES, INSECT; DROSOPHILA; GENE FLOW; GENES, INSECT; GENES, MITOCHONDRIAL; GENETIC SPECIATION; POLYMORPHISM, GENETIC; Y CHROMOSOME;

EID: 84896718070     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12295     Document Type: Article

References (169)

1. Andolfatto, P. 2001. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 18:279-290.
2. Arnold, M. L. 1997. Natural hybridization and evolution. Oxford Univ. Press, Oxford, U.K.
3. Arnold, M. L. 2006. Evolution through genetic exchange. Oxford Univ. Press, Oxford, U.K.
4. Arnold, M. L., and N. H. Martin. 2009. Adaptation by introgression. J. Biol. 8:82.
5. Ayala, F. J., L. Serra, and A. Prevosti. 1989. A grand experiment in evolution: the Drosophila subobscura colonization of the Americas. Genome 31:246-255.
6. Bachtrog, D., K. Thornton, A.A. Clark, and P. Andolfatto. 2006. Extensive introgression of mitochondrial DNA relative to nuclear genes in the Drosophila yakuba species group. Evolution 60:292-302.
7. Baines, J. F., and B. Harr. 2007. Reduced X-linked diversity in derived populations of house mice. Genetics 175:1911-1921.
8. Ballard, J. W. 2000. When one is not enough: introgression of mitochondrial DNA in Drosophila. Mol. Biol. Evol. 17:1126-1130.
9. Ballard, J. W. O., and M. C. Whitlock. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13:729-744.
10. Barton, N., and J. S. Jones. 1983. Evolutionary biology. Mitochondrial DNA: new clues about evolution. Nature 306:317-318.
11. Barton, N. H., and G. M. Hewitt. 1981a. A chromosomal cline in the grasshopper Podisma pedestris. Evolution 35:1008-1018.
12. Barton, N. H., and G. M. Hewitt. 1981b. Hybrid zones and speciation. Pp. 109-145 in W. R. Atchley and D. S. Woodruf, eds. Evolution and speciation. Cambridge Univ. Press, Cambridge, U.K.
13. Becquet, C., and M. Przeworski. 2007. A new approach to estimate parameters of speciation models with application to apes. Genome Res. 17:1505-1519.
14. Begun, D. J., and C. F. Aquadro. 1993. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature 365:548-550.
15. Begun, D. J., A. K. Holloway, K. Stevens, L. W. Hillier, Y. P. Poh, M. W. Hahn, P. M. Nista, C. D. Jones, A. D. Kern, C. N. Dewey, et al. 2007. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5:e310.
16. Begun, D. J., and P. Whitley. 2000. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc. Natl. Acad. Sci. USA 97:5960-5965.
17. Blier, P. U., F. Dufresne, and R. S. Burton. 2001. Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17:400-406.
18. Braverman, J. M., R. R. Hudson, N. L. Kaplan, C. H. Langley, and W. Stephan. 1995. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783-796.
19. Burton, R. S., and F. S. Barreto. 2012. A disproportionate role for mtDNA in Dobzhansky-Muller incompatibilities? Mol. Ecol. 21:4942-4957.
20. Cariou, M. L., D. Lachaise, L. Tsacas, J. Sourdis, C. B. Krimbas, and M. Ashburner. 1988. New African species in the Drosophila obscura species group: genetic variation, differentiation and evolution. Heredity 61:73-84.
21. Carneiro, M., J. A. Blanco-Aguiar, R. Villafuerte, N. Ferrand, and M. W. Nachman. 2010. Speciation in the European rabbit (Oryctolagus cuniculus): islands of differentiation on the X chromosome and autosomes. Evolution 64:3443-3460.
22. Carvalho, A. B., and A. G. Clark. 2005. Y chromosome of D. pseudoobscura is not homologous to the ancestral Drosophila Y. Science 307:108-110.
23. Castric, V., J. Bechsgaard, M. H. Schierup, and X. Vekemans. 2008. Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet. 4:e1000168.
24. Castro, J. A., M. Ramon, A. Picornell, and A. Moya. 1999. The genetic structure of Drosophila subobscura populations from the Islands of Majorca and Minorca (Balearic Islands, Spain) based on allozymes and mitochondrial DNA. Heredity (Edinb.) 83(Pt 3):271-279.
25. Charlesworth, B. 2012a. The effects of deleterious mutations on evolution at linked sites. Genetics 190:5-22.
26. Charlesworth, B. 2012b. The role of background selection in shaping patterns of molecular evolution and variation: evidence from variability on the Drosophila X chromosome. Genetics 191:233-246.
27. Charlesworth, B., J. A. Coyne, and N. Barton. 1987. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130:113-146.
28. Charlesworth, B., M. T. Morgan, and D. Charlesworth. 1993a. The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
29. Charlesworth, D., M. T. Morgan, and B. Charlesworth. 1993b. Mutation accumulation in finite outbreeding and inbreeding populations. Genet. Res. 61:39-56.
30. Comeron, J. M., and M. Kreitman. 2002. Population, evolutionary and genomic consequences of interference selection. Genetics 161:389-410.
31. Connallon, T., N. D. Singh, and A. G. Clark. 2012. Impact of genetic architecture on the relative rates of X versus autosomal adaptive substitution. Mol. Biol. Evol. 29:1933-1942.
32. Counterman, B. A., and M. A. Noor. 2006. Multilocus test for introgression between the cactophilic species Drosophila mojavensis and Drosophila arizonae. Am. Nat. 168:682-696.
33. Coyne, J. A. 1985. The genetic basis of Haldane's rule. Nature 314:736-738.
34. Coyne, J. A. 1992. Genetics and speciation. Nature 355:511-515.
35. Coyne, J. A., S. Elwyn, S. Y. Kim, and A. Llopart. 2004. Genetic studies of two sister species in the Drosophila melanogaster subgroup, D. yakuba and D. santomea. Genet. Res. 84:11-26.
36. Coyne, J. A., and H. A. Orr. 1989. Two rules of speciation. Pp. 180-207 in D. Otte and J. Endler, eds. Speciation and its consequences. Sinauer Associates, Sunderland, MA.
37. Coyne, J. A., and H. A. Orr. 1998. The evolutionary genetics of speciation. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353:287-305.
38. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
39. Dobzhansky, T. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
40. Dod, B., L. S. Jermiin, P. Boursot, V. H. Chapman, J. T. Nielsen, and F. Bonhomme. 1993. Counterselection on sex-chromosomes in the Mus musculus European hybrid zone. J. Evol. Biol. 6:529-546.
41. Dowling, D. K., U. Friberg, and J. Lindell. 2008. Evolutionary implications of non-neutral mitochondrial genetic variation. Trends Ecol. Evol. 23:546-554.
42. Faria, R., and A. Navarro. 2010. Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol. Evol. 25:660-669.
43. Fay, J. C., and C. I. Wu. 1999. A human population bottleneck can account for the discordance between patterns of mitochondrial versus nuclear DNA variation. Mol. Biol. Evol. 16:1003-1005.
44. Felsenstein, J. 1985. Phylogenies and the Comparative Method. Am. Nat. 125:1-15.
45. Ferris, S. D., R. D. Sage, C. M. Huang, J. T. Nielsen, U. Ritte, and A. C. Wilson. 1983. Flow of mitochondrial DNA across a species boundary. Proc. Natl. Acad. Sci. USA 80:2290-2294.
46. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925.
47. Garrigan, D., S. B. Kingan, A. J. Geneva, P. Andolfatto, A. G. Clark, K. R. Thornton, and D. C. Presgraves. 2012. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res. 22:1499-1511.
48. Gay, J., S. Myers, and G. McVean. 2007. Estimating meiotic gene conversion rates from population genetic data. Genetics 177:881-894.
49. Geraldes, A., P. Basset, B. Gibson, K. L. Smith, B. Harr, H. T. Yu, N. Bulatova, Y. Ziv, and M. W. Nachman. 2008a. Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol. Ecol. 17:5349-5363.
50. Geraldes, A., M. Carneiro, M. Delibes-Mateos, R. Villafuerte, M. W. Nachman, and N. Ferrand. 2008b. Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula. Mol. Ecol. 17:4489-4499.
51. Gillespie, J. H. 2001. Is the population size of a species relevant to its evolution? Evolution 55:2161-2169.
52. Gonzalez, A. M., M. Hernandez, A. Volz, J. Pestano, J. M. Larruga, D. Sperlich, and V. M. Cabrera. 1990. Mitochondrial DNA evolution in the obscura species subgroup of Drosophila. J. Mol. Evol. 31:122-131.
53. Gordo, I., A. Navarro, and B. Charlesworth. 2002. Muller's ratchet and the pattern of variation at a neutral locus. Genetics 161:835-848.
54. Haag-Liautard, C., N. Coffey, D. Houle, M. Lynch, B. Charlesworth, and P. D. Keightley. 2008. Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biol. 6:e204.
55. Hadany, L., and J. M. Comeron. 2008. Why are sex and recombination so common? Ann. N Y Acad. Sci. 1133:26-43.
56. Haddrill, P. R., L. Loewe, and B. Charlesworth. 2010. Estimating the parameters of selection on nonsynonymous mutations in Drosophila pseudoobscura and D. miranda. Genetics 185:1381-1396.
57. Harrison, R. H. 1990. Hybrid zones: windows on evolutionary processes. Oxf. Surv. Evol. Biol. 7:69-128.
58. Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
59. Hewitt, G. M. 1988. Hybrid zones-Natural laboratories for evolutionary studies. Trends. Ecol. Evol. 3:158-167.
60. Hey, J. 2001. Genes, categories, and species. Oxford Univ. Press, New York.
61. Hey, J. 2006. Recent advances in assessing gene flow between diverging populations and species. Curr. Opin. Genet. Dev. 16:592-596.
62. Hey, J. 2010. The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses. Mol. Biol. Evol. 27:921-933.
63. Hey, J., and R. Nielsen. 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747-760.
64. Hey, J., and R. Nielsen. 2007. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. USA 104:2785-2790.
65. Hey, J., and C. Pinho. 2012. Population genetics and objectivity in species diagnosis. Evolution 66:1413-1429.
66. Hudson, R. R. 2000. A new statistic for detecting genetic differentiation. Genetics 155:2011-2014.
67. Hudson, R. R., and N. L. Kaplan. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147-164.
68. Hudson, R. R., M. Kreitman, and M. Aguade. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
69. Hudson, R. R., M. Slatkin, and W. P. Maddison. 1992. Estimation of levels of gene flow from DNA sequence data. Genetics 132:583-589.
70. Hutter, S., H. Li, S. Beisswanger, D. De Lorenzo, and W. Stephan. 2007. Distinctly different sex ratios in African and European populations of Drosophila melanogaster inferred from chromosomewide single nucleotide polymorphism data. Genetics 177:469-480.
71. Kaplan, N. L., R. R. Hudson, and C. H. Langley. 1989. The "hitchhiking effect" revisited. Genetics 123:887-899.
72. Khadem, M., R. Camacho, and C. Nobrega. 2011. Studies of the species barrier between Drosophila subobscura and D. madeirensis V: the importance of sex-linked inversion in preserving species identity. J. Evol. Biol. 24:1263-1273.
73. Khadem, M., and C. B. Krimbas. 1991. Studies of the species barrier between Drosophila subobscura and D. madeirensis. I. The genetics of male hybrid sterility. Heredity 67:157-165.
74. Khadem, M., A. Munte, R. Camacho, M. Aguade, and C. Segarra. 2012. Multilocus analysis of nucleotide variation in Drosophila madeirensis, an endemic species of the Laurisilva forest in Madeira. J. Evol. Biol. 25:726-739.
75. Kim, M., M. L. Cui, P. Cubas, A. Gillies, K. Lee, M. A. Chapman, R. J. Abbott, and E. Coen. 2008. Regulatory genes control a key morphological and ecological trait transferred between species. Science 322:1116-1119.
76. Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-120.
77. Kliman, R. M., P. Andolfatto, J. A. Coyne, F. Depaulis, M. Kreitman, A. J. Berry, J. McCarter, J. Wakeley, and J. Hey. 2000. The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156:1913-1931.
78. Krimbas, C. B., and M. Loukas. 1984. Evolution of the obscura group Drosophila species. I. Salivary chromosomes and quantitative characters in D. subobscura and two closely related species. Heredity 53:469-482.
79. Lakovaara, S., and A. Saura. 1982. Evolution and speciation in the Drosophila obscura group. Pp. 1-59 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Academic Press, Inc., New York.
80. Langley, C. H., K. Stevens, C. Cardeno, Y. C. Lee, D. R. Schrider, J. E. Pool, S. A. Langley, C. Suarez, R. B. Corbett-Detig, B. Kolaczkowski, 2012. Genomic variation in natural populations of Drosophila melanogaster. Genetics 192:533-598.
81. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
82. Larracuente, A. M., and A. G. Clark. 2013. Surprising differences in the variability of Y chromosomes in African and cosmopolitan populations of Drosophila melanogaster. Genetics 193:201-214.
83. Larruga, J. M., V. M. Cabrera, A. M. Gonzalez, and A. Gullon. 1983. Molecular and chromosomal polymorphism in continental and insular populations from the southwestern range of Drosophila subobscura. Genetica 60:191-205.
84. Leffler, E. M., K. Bullaughey, D. R. Matute, W. K. Meyer, L. Segurel, A. Venkat, P. Andolfatto, and M. Przeworski. 2012. Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10:e1001388.
85. Lewontin, R. C. 1974. The genetic basis of evolutionary change. Columbia Univ. Press, New York.
86. Li, S., Y. Chen, H. Gao, and T. Yin. 2010. Potential chromosomal introgression barriers revealed by linkage analysis in a hybrid of Pinus massoniana and P. hwangshanensis. BMC Plant Biol. 10:37.
87. Librado, P., and J. Rozas. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452.
88. Llopart, A. 2012. The rapid evolution of X-linked male-biased gene expression and the large-X effect in Drosophila yakuba, D. santomea and their hybrids. Mol. Biol. Evol. 29:3873-3886.
89. Llopart, A., S. Elwyn, D. Lachaise, and J. A. Coyne. 2002. Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea. Evol. Int. J. Org. Evol. 56:2262-2277.
90. Llopart, A., D. Lachaise, and J. A. Coyne. 2005. Multilocus analysis of introgression between two sympatric sister species of Drosophila: Drosophila yakuba and D. santomea. Genetics 171:197-210.
91. Loukas, M., C. B. Krimbas, P. Mavragani-Tsipidou, and C. D. Kastritsis. 1979. Genetics of Drosophila subobscura populations. VIII. Allozyme loci and their chromosome maps. J. Hered. 70:17-26.
92. Lynch, M., and W. Gabriel. 1990. Mutation load and the survival of small populations. Evolution 44:1725-1737.
93. Machado, C. A., and J. Hey. 2003. The causes of phylogenetic conflict in a classic Drosophila species group. Proc. R. Soc. Lond. B Biol. Sci. 270:1193-1202.
94. Machado, C. A., R. M. Kliman, J. A. Markert, and J. Hey. 2002. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives. Mol. Biol. Evol. 19:472-488.
95. Macholan, M., P. Munclinger, M. Sugerkova, P. Dufkova, B. Bimova, E. Bozikova, J. Zima, and J. Pialek. 2007. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61:746-771.
96. Mackay, T. F., S. Richards, E. A. Stone, A. Barbadilla, J. F. Ayroles, D. Zhu, S. Casillas, Y. Han, M. M. Magwire, J. M. Cridland, et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173-178.
97. Mallet, J. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20:229-237.
98. Mateos, M., S. J. Castrezana, B. J. Nankivell, A. M. Estes, T. A. Markow, and N. A. Moran. 2006. Heritable endosymbionts of Drosophila. Genetics 174:363-376.
99. Maynard Smith, J., and J. Haigh. 1974. The hitch-hiking effect of a favorable gene. Genet. Res. 23:23-35.
100. Mayr, E. 1942. Systematics and the origin of species. Columbia Univ. Press, New York.
101. Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
102. McDermott, S. R., and R. M. Kliman. 2008. Estimation of isolation times of the island species in the Drosophila simulans complex from multilocus DNA sequence data. PLoS ONE 3:e2442.
103. McDonald, J. H., and M. Kreitman. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
104. Meiklejohn, C. D., M. A. Holmbeck, M. A. Siddiq, D. N. Abt, D. M. Rand, and K. L. Montooth. 2013. An Incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9:e1003238.
105. Meisel, R. P., J. H. Malone, and A. G. Clark. 2012. Faster-X evolution of gene expression in Drosophila. PLoS Genet. 8:e1003013.
106. Mestres, F., J. Balanya, C. Arenas, E. Sole, and L. Serra. 2001. Colonization of America by Drosophila subobscura: heterotic effect of chromosomal arrangements revealed by the persistence of lethal genes. Proc. Natl. Acad. Sci. USA 98:9167-9170.
107. Molto, M. D., M. J. Martinez-Sebastian, and R. De Frutos. 1994. Phylogenetic relationships between Drosophila subobscura, D. guanche and D. madeirensis based on Southern analysis of heat shock genes. Hereditas 120:217-223.
108. Monclus, M. 1984. Drosophilidae of Madeira, with the description of Drosophila madeirensis n. sp. Z. Zool. Syst. Evol. 22:94-103.
109. Moriyama, E. N., and J. R. Powell. 1997. Synonymous substitution rates in Drosophila: mitochondrial versus nuclear genes. J. Mol. Evol. 45:378-391.
110. Muller, H. J. 1940. Bearing of the Drosophila work on systematics. Pp. 185-268 in J. S. Huxley, ed. The new systematics. Clarendon Press, Oxford, U.K.
111. Nabholz, B., H. Ellegren, and J. B. Wolf. 2013. High levels of gene expression explain the strong evolutionary constraint of mitochondrial protein-coding genes. Mol. Biol. Evol. 30:272-284.
112. Navarro, A., and N. H. Barton. 2003a. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447-459.
113. Navarro, A., and N. H. Barton. 2003b. Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes. Science 300:321-324.
114. Nielsen, R., and J. Wakeley. 2001. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885-896.
115. Noor, M. A., D. A. Garfield, S. W. Schaeffer, and C. A. Machado. 2007. Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. Genetics 177:1417-1428.
116. Noor, M. A., K. L. Grams, L. A. Bertucci, and J. Reiland. 2001. Chromosomal inversions and the reproductive isolation of species. Proc. Natl. Acad. Sci. USA 98:12084-12088.
117. Nowell, R. W., B. Charlesworth, and P. R. Haddrill. 2011. Ancestral polymorphisms in Drosophila pseudoobscura and Drosophila miranda. Genet. Res. (Camb.) 93:255-263.
118. Nunes, M. D., P. O. Wengel, M. Kreissl, and C. Schlotterer. 2010. Multiple hybridization events between Drosophila simulans and Drosophila mauritiana are supported by mtDNA introgression. Mol. Ecol. 19:4695-4707.
119. Oliver, P., J. A. Castro, A. Picornell, M. M. Ramon, E. Sole, J. Balanya, L. Serra, A. Latorre, and A. Moya. 2002. Linkage disequilibria between mtDNA haplotypes and chromosomal arrangements in a natural population of Drosophila subobscura. Heredity (Edinb.) 89:133-138.
120. Osada, N., and H. Akashi. 2012. Mitochondrial-nuclear interactions and accelerated compensatory evolution: evidence from the primate cytochrome C oxidase complex. Mol. Biol. Evol. 29:337-346.
121. Papaceit, M., M. Aguade, and C. Segarra. 2006. Chromosomal evolution of elements B and C in the Sophophora subgenus of Drosophila: evolutionary rate and polymorphism. Evolution 60:768-781.
122. Papaceit, M., and A. Prevosti. 1989. Differences in chromosome A arrangement between Drosophila madeirensis and Drosophila subobscura. Experientia 45:310-312.
123. Papaceit, M., and A. Prevosti. 1991. A photographic map of Drosophila madeirensis polytene chromosomes. J. Hered. 82:471-478.
124. Papaceit, M., J. San Antonio, and A. Prevosti. 1991. Genetic analysis of extra sex combs in the hybrids between Drosophila subobscura and D. madeirensis. Genetica 84:107-114.
125. Pardo-Diaz, C., C. Salazar, S. W. Baxter, C. Merot, W. Figueiredo-Ready, M. Joron, W. O. McMillan, and C. D. Jiggins. 2012. Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genet. 8:e1002752.
126. Payseur, B. A., J. G. Krenz, and M. W. Nachman. 2004. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58:2064-2078.
127. Pegueroles, C., P. A. Arauz, M. Pascual, and F. Mestres. 2010. A recombination survey using microsatellites: the O chromosome of Drosophila subobscura. Genetica 138:795-804.
128. Pinho, C., and J. Hey. 2010. Divergence with gene flow: models and data. Annu. Rev. Ecol. Evol. Syst. 41:215-230.
129. Pool, J. E., and R. Nielsen. 2007. Population size changes reshape genomic patterns of diversity. Evolution 61:3001-3006.
130. Powell, J. R. 1983. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc. Natl. Acad. Sci. USA 80:492-495.
131. Ramos-Onsins, S., C. Segarra, J. Rozas, and M. Aguade. 1998. Molecular and chromosomal phylogeny in the obscura group of Drosophila inferred from sequences of the rp49 gene region. Mol. Phylogenet. Evol. 9:33-41.
132. Ramos-Onsins, S. E., B. E. Stranger, T. Mitchell-Olds, and M. Aguade. 2004. Multilocus analysis of variation and speciation in closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373-388.
133. Rand, D. M., R. A. Haney, and A. J. Fry. 2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19:645-653.
134. Rieseberg, L. 2011. Adaptive introgression: the seeds of resistance. Curr. Biol. 21:R581-R583.
135. Rieseberg, L. H. 2001. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16:351-358.
136. Rieseberg, L. H. 2009. Evolution: replacing genes and traits through hybridization. Curr. Biol. 19:R119-R122.
137. Rozas, J., and M. Aguade. 1990. Evidence of extensive genetic exchange in the rp49 region among polymorphic chromosome inversions in Drosophila subobscura. Genetics 126:417-426.
138. Rozas, J., M. Hernandez, V. M. Cabrera, and A. Prevosti. 1990. Colonization of America by Drosophila subobscura: effect of the founder event on the mitochondrial DNA polymorphism. Mol. Biol. Evol. 7:103-109.
139. Sackton, T. B., H. Montenegro, D. L. Hartl, and B. Lemos. 2011. Interspecific Y chromosome introgressions disrupt testis-specific gene expression and male reproductive phenotypes in Drosophila. Proc. Natl. Acad. Sci. USA 108:17046-17051.
140. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:404-425.
141. Schaeffer, S. W., A. Bhutkar, B. F. McAllister, M. Matsuda, L. M. Matzkin, P. M. O'Grady, C. Rohde, V. L. Valente, M. Aguade, and W. W. Anderson. 2008. Polytene chromosomal maps of 11 Drosophila species: the order of genomic scaffolds inferred from genetic and physical maps. Genetics 179:1601-1655.
142. Segarra, C., and M. Aguade. 1992. Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics 130:513-521.
143. Segarra, C., G. Ribo, and M. Aguade. 1996. Differentiation of Muller's chromosomal elements D and E in the obscura group of Drosophila. Genetics 144:139-146.
144. Simonsen, K. L., G. A. Churchill, and C. F. Aquadro. 1995. Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413-429.
145. Singh, N. D., J. M. Macpherson, J. D. Jensen, and D. A. Petrov. 2007. Similar levels of X-linked and autosomal nucleotide variation in African and non-African populations of Drosophila melanogaster. BMC Evol. Biol. 7:202.
146. Song, Y., S. Endepols, N. Klemann, D. Richter, F. R. Matuschka, C. H. Shih, M. W. Nachman, and M. H. Kohn. 2011. Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Curr. Biol. 21:1296-1301.
147. Sota, T., and A. P. Vogler. 2001. Incongruence of mitochondrial and nuclear gene trees in the Carabid beetles Ohomopterus. Syst. Biol. 50:39-59.
148. Staubach, F., A. Lorenc, P. W. Messer, K. Tang, D. A. Petrov, and D. Tautz. 2012. Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus). PLoS Genet. 8:e1002891.
149. Stephan, W. 2010. Genetic hitchhiking versus background selection: the controversy and its implications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365:1245-1253.
150. Stephan, W., Y. S. Song, and C. H. Langley. 2006. The hitchhiking effect on linkage disequilibrium between linked neutral loci. Genetics 172:2647-2663.
151. Stephens, M., and P. Scheet. 2005. Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am. J. Hum. Genet. 76:449-462.
152. Stevison, L. S., K. B. Hoehn, and M. A. Noor. 2011. Effects of inversions on within- and between-species recombination and divergence. Genome Biol. Evol. 3:830-841.
153. Strasburg, J. L., and L. H. Rieseberg. 2010. How robust are "isolation with migration" analyses to violations of the IM model? A simulation study. Mol. Biol. Evol. 27:297-310.
154. Sturtevant, A. H., and E. Novitski. 1941. The homologies of the chromosome elements in the genus Drosophila. Genetics 26:517-541.
155. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
156. Tamura, K., and S. Kumar. 2002. Evolutionary distance estimation under heterogeneous substitution pattern among lineages. Mol. Biol. Evol. 19:1727-1736.
157. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
158. Tamura, K., S. Subramanian, and S. Kumar. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21:36-44.
159. Teeter, K. C., B. A. Payseur, L. W. Harris, M. A. Bakewell, L. M. Thibodeau, J. E. O'Brien, J. G. Krenz, M. A. Sans-Fuentes, M. W. Nachman, and P. K. Tucker. 2008. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18:67-76.
160. Tucker, P. K., R. D. Sage, J. Warner, A. C. Wilson, and E. M. Eicher. 1992. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46:1146-1163.
161. Untergasser, A., H. Nijveen, X. Rao, T. Bisseling, R. Geurts, and J. A. Leunissen. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 35:W71-74.
162. Vicoso, B., and B. Charlesworth. 2009. Effective population size and the faster-X effect: an extended model. Evolution 63:2413-2426.
163. Volz-Lingenhohl, A., M. Solignac, and D. Sperlich. 1992. Stable heteroplasmy for a large-scale deletion in the coding region of Drosophila subobscura mitochondrial DNA. Proc. Natl. Acad. Sci. USA 89:11528-11532.
164. Whitney, K. D., R. A. Randell, and L. H. Rieseberg. 2006. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am. Nat. 167:794-807.
165. Wiehe, T. H., and W. Stephan. 1993. Analysis of a genetic hitchhiking model, and its application to DNA polymorphism data from Drosophila melanogaster. Mol. Biol. Evol. 10:842-854.
166. Won, Y. J., and J. Hey. 2005. Divergence population genetics of chimpanzees. Mol. Biol. Evol. 22:297-307.
167. Wu, C. I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14:851-865.
168. Yang, Z. 2010. A likelihood ratio test of speciation with gene flow using genomic sequence data. Genome Biol. Evol. 2:200-211.
169. Zurovcova, M., and W. F. Eanes. 1999. Lack of nucleotide polymorphism in the Y-linked sperm flagellar dynein gene Dhc-Yh3 of Drosophila melanogaster and D. simulans. Genetics 153:1709-1715.