Coalescent patterns for chromosomal inversions in divergent populations

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 367, Issue 1587, 2012, Pages 430-438

  Guerrero, Rafael F ^a   Rousset, François ^b   Kirkpatrick, Mark ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b INSTITUT DES SCIENCES DE L EVOLUTION   (France)

Author keywords

Chromosomal inversions; Coalescent models; Genetic variation; Local adaptation; Recombination

Indexed keywords

ALLELE; CHROMOSOME; DIVERGENCE; EVOLUTIONARY BIOLOGY; GENETIC DRIFT; GENETIC VARIATION; GENOMICS; HYBRIDIZATION; LOCAL ADAPTATION; POLYMORPHISM; SPECIATION (BIOLOGY);

EID: 84255162265     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0246     Document Type: Article

References (68)

1. Hoffmann, A. & Rieseberg, L. 2008 Revisiting the impact of inversions in evolution: from population genetic markers to drivers of adaptive shifts and speciation? Annu. Rev. Ecol. Evol. Syst. 39, 21. (doi:10.1146/annurev.ecolsys.39.110707.173532)
2. Kirkpatrick, M. 2010 How and why chromosome inversions evolve. PLoS Biol. 8, 1000501. (doi:10.1371/journal.pbio.1000501)
3. Dobzhansky, T. 1951 Genetics and the origin of species (eds N. Eldredge & S. J. Gould), 3rd edn. New York, NY: Columbia University Press.
4. rd edn. Cambridge, UK: Cambridge University Press.
5. Sandler, L. & Hiraizumi, Y. 1960 Meiotic drive in natural populations of Drosophila melanogaster. IV. Instability at the segregation-distorter locus. Genetics 45, 1269-1287.
6. White, M. J. D. 1969 Chromosomal rearrangements and speciation in animals. Annu. Rev. Genet. 3, 75-98. (doi:10.1146/annurev.ge.03.120169.000451)
7. White, M. J. D. 1978 Modes of speciation. San Francisco, CA: W.H. Freeman.
8. Coyne, J. A. & Orr, H. A. 2004 Speciation. Sunderland, MA: Sinauer Associates, Inc.
9. Barton, N. H. & Charlesworth, B. 1984 Genetic revolutions, founder effects, and speciation. Annu. Rev. Ecol. Syst. 15, 133-164. (doi:10.1146/annurev.es.15.110184.001025)
10. Coyne, J. A., Meyers, W., Crittenden, A. P. & Sniegowski, P. 1993 The fertility effects of pericentric inversions in Drosophila melanogaster. Genetics 134, 487-496.
11. Noor, M. A. F., Grams, K. L., Bertucci, L. A. & Reiland, J. 2001 Chromosomal inversions and the reproductive isolation of species. Proc. Natl Acad. Sci. USA 98, 12084-12088. (doi:10.1073/pnas.221274498)
12. Rieseberg, L. H. 2001 Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351-358. (doi:10.1016/S0169-5347(01)02187-5)
13. Ortiz-Barrientos, D., Reiland, J., Hey, J. & Noor, M. A. 2002 Recombination and the divergence of hybridizing species. Genetica 116, 167-178. (doi:10.1023/A:1021296829109)
14. Sturtevant, A. H. & Beadle, G. W. 1936 The relations of inversions in the X chromosome of Drosophila melanogaster to crossing over and disjunction. Genetics 21, 554-604.
15. Navarro, A. & Barton, N. H. 2003 Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57, 447-459.(doi:10.1111/j.0014-3820.2003.tb01537.x)
16. Feder, J. L. & Nosil, P. 2009 Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution 63, 3061-3075.(doi:10.1111/j.1558-5646.2009.00786.x)
17. Charlesworth, D. & Charlesworth, B. 1979 Selection on recombination in clines. Genetics 91, 581-589.
18. Kirkpatrick, M. & Barton, N. 2006 Chromosome inversions, local adaptation and speciation. Genetics 173, 419.(doi:10.1534/genetics.105.047985)
19. Nosil, P. & Feder, J. L. 2012 Genomic divergence during speciation: causes and consequences. Phil. Trans. R. Soc. B 367, 332-342. (doi:10.1098/rstb.2011.0263)
20. Brown, K. M., Burk, L. M., Henagan, L. M. & Noor, M. A. 2004 A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura. Evolution 58, 1856-1860. (doi:10.1111/j.0014-3820.2004.tb00469.x)
21. Livingstone, K. & Rieseberg, L. 2004 Chromosomal evolution and speciation: a recombination-based approach. New Phytologist 161, 107-112. (doi:10.1046/j.1469-8137.2003.00942.x)
22. Noor, M. A. F., Garfield, D. A., Schaeffer, S. W. & Machado, C. A. 2007 Divergence between the Drosophila pseudoobscura and D. persimilis genome sequences in relation to chromosomal inversions. Genetics 177,1417-1428. (doi:10.1534/genetics.107.070672)
23. Yatabe, Y., Kane, N. C., Scotti-Saintagne, C. & Rieseberg, L. H. 2007 Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175, 1883-1893. (doi:10.1534/genetics.106.064469)
24. Schaeffer, S.W., Goetting-Minesky, M. P., Kovacevic, M., Peoples, J. R., Graybill, J. L., Miller, J. M., Kim, K., Nelson, J. G. & Anderson, W.W. 2003 Evolutionary genomics of inversions in Drosophila pseudoobscura: evidence for epistasis. Proc. Natl Acad. Sci. USA 100, 8319-8324.(doi:10.1073/pnas.1432900100)
25. Michel, A. P., Sim, S., Powell, T. H. Q., Taylor, M. S., Nosil, P. & Feder, J. L. 2010 Widespread genomic divergence during sympatric speciation. Proc. Natl Acad. Sci. USA 107, 9724-9729. (doi:10.1073/Pnas.1000939107)
26. White, B. J., Hahn, M. W., Pombi, M., Cassone, B. J., Lobo, N. F., Simard, F. & Besansky, N. J. 2007 Localization of candidate regions maintaining a common polymorphic inversion (2La) in Anopheles gambiae. PLoS Genet. 3, 217. (doi:10.1371/journal.pgen.0030217)
27. Kennington, W. J., Partridge, L. & Hoffmann, A. A. 2006 Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation. Genetics 172, 1655-1663. (doi:10.1534/genetics.105.053173)
28. Matzkin, L., Merritt, T., Zhu, C. & Eanes, W. 2005 The structure and population genetics of the breakpoints associated with the cosmopolitan chromosomal inversion In(3R)Payne in Drosophila melanogaster. Genetics 170, 1143-1152. (doi:10.1534/genetics.104.038810)
29. Tsuchimatsu, T. et al. 2010 Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464, 1342-1346. (doi:10.1038/nature08927)
30. Puig, M., Caceres, M. & Ruiz, A. 2004 Silencing of a gene adjacent to the breakpoint of a widespread Drosophila inversion by a transposon-induced antisense RNA. Proc. Natl Acad. Sci. USA 101, 9013-9018. (doi:10.1073/pnas.0403090101)
31. Munté, A., Rozas, J., Aguadé, M. & Segarra, C. 2005 Chromosomal inversion polymorphism leads to extensive genetic structure: a multilocus survey in Drosophila subobscura. Genetics 169, 1573-1581. (doi:10.1534/genetics.104.032748)
32. Cohuet, A., Dia, I., Simard, F., Raymond, M. & Fontenille, D. 2004 Population structure of the malaria vector Anopheles funestus in Senegal based on microsatellite and cytogenetic data. Insect Mol. Biol. 13, 251-258.(doi:10.1111/j.0962-1075.2004.00482.x)
33. White, B. J., Cheng, C., Sangaré, D., Lobo, N. F., Collins, F. H. & Besansky, N. J. 2009 The population genomics of trans-specific inversion polymorphisms in Anopheles gambiae. Genetics 183, 275-288. (doi:10.1534/genetics.109.105817)
34. Navarro, A., Betran, E., Barbadilla, A. & Ruiz, A. 1997 Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146, 695-709.
35. Schaeffer, S.W. & Anderson, W.W. 2005 Mechanisms of genetic exchange within the chromosomal inversions of Drosophila pseudoobscura. Genetics 171, 1729-1739.(doi:10.1534/genetics.105.041947)
36. Navarro, A., Barbadilla, A. & Ruiz, A. 2000 Effect of inversion polymorphism on the neutral nucleotide variability of linked chromosomal regions in Drosophila. Genetics 155, 685-698.
37. Wakeley, J. 2009 Coalescent theory: an introduction. Greenwood Village, CO: Roberts and Company.
38. Nagylaki, T. 1980 The strong-migration limit in geographically structured populations. J. Math. Biol. 9, 101-114. (doi:10.1007/BF00275916)
39. Wolfram Research, I 2008 Mathematica, v. 70 edn. Campaign, IL: Wolfram Research, Inc.
40. Kaplan, N. L., Hudson, R. R. & Langley, C. H. 1989 The 'hitchhiking effect' revisted. Genetics 123,887-899.
41. Kim, Y. & Stephan, W. 2002 Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160, 765-777.
42. Machado, C. A., Haselkorn, T. S. & Noor, M. A. F. 2007 Evaluation of the genomic extent of effects of fixed inversion differences on intraspecific variation and interspecific gene flow in Drosophila pseudoobscura and D. persimilis. Genetics 175, 1289-1306. (doi:10.1534/Genetics.106.064758)
43. Nordborg, M. 1997 Structured coalescent processes on different time scales. Genetics 146, 1501-1514.
44. Chovnick, A. 1973 Gene conversion and transfer of genetic information within the inverted region of inversion heterozygotes. Genetics 75, 123-131.
45. Payne, F. 1924 Crossover modifiers in the third chromosome of Drosophila melanogaster. Genetics 9, 327-342.
46. Kaplan, N., Hudson, R. R. & Iizuka, M. 1991 The coalescent process in models with selection, recombination and geographic subdivision. Genet. Res. 57, 83-91.(doi:10.1017/S0016672300029074)
47. Wright, S. 1951 The genetical structure of populations. Ann. Eugen. 15, 323-354. (doi:10.1111/j.1469-1809.1949.tb02451.x)
48. Slatkin, M. 1991 Inbreeding coefficients and coalescence times. Genet. Res. 58, 167-175. (doi:10.1017/S0016672300029827)
49. Hudson, R. R. & Kaplan, N. L. 1988 The coalescent process in models with selection and recombination. Genetics 120, 831-840.
50. Kaplan, N. L., Darden, T. & Hudson, R. R. 1988 The coalescent process in models with selection. Genetics 120, 819-820.
51. Andolfatto, P., Depaulis, F. & Navarro, A. 2001 Inversion polymorphisms and nucleotide variability in Drosophila. Genet. Res. 77, 1-8. (doi:10.1017/S0016672301004955)
52. Przeworski, M., Coop, G. & Wall, J. 2005 The signature of positive selection on standing genetic variation. Evolution 59, 2312-2323. (doi:10.1111/j.0014-3820.2005.tb00941.x)
53. Kimura, M. & Ohta, T. 1971 Theoretical topics in population genetics. Princeton, NJ: Princeton University Press.
54. Gillespie, J. H. 2000 Genetic drift in an infinite population: the pseudohitchhiking model. Genetics 155, 909-919.
55. Barton, N. H. 2000 Genetic hitchhiking. Phil. Trans. R. Soc. Lond. B 355, 1553-1562. (doi:10.1098/rstb.2000.0716)
56. White, B. J., Cheng, C., Simard, F., Costantini, C. & Besansky, N. J. 2010 Genetic association of physically unlinked islands of genomic divergence in incipient species of Anopheles gambiae. Mol. Ecol. 19, 925-939.(doi:10.1111/j.1365-294X.2010.04531.x)
57. Stump, A. D., Pombi, M., Goeddel, L., Ribeiro, J. M. C., Wilder, J. A., Torre, A. D. & Besansky, N. J. 2007 Genetic exchange in 2La inversion heterokaryotypes of Anopheles gambiae. Insect Mol. Biol. 16, 703-709. (doi:10.1111/j.1365-2583.2007.00764.x)
58. Onyabe, D. Y. & Conn, J. E. 2001 Genetic differentiation of the malaria vector Anopheles gambiae across Nigeria suggests that selection limits gene flow. Heredity 87, 647-658. (doi:10.1046/j.1365-2540.2001.00957.x)
59. Feder, J. L. & Nosil, P. 2010 The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64, 1729-1747. (doi:10.1111/j.1558-5646.2010.00943.x)
60. Via, S. 2012 Divergence hitchhiking and the spread of genomic isolation during ecological speciation-withgene- flow. Phil. Trans. R. Soc. B 367, 451-460.(doi:10.1098/rstb.2011.0260)
61. Charlesworth, B., Nordborg, M. & Charlesworth, D. 1997 The effects of local selection, balanced polymorphism and background selection on equilibrium patterns of genetic diversity in subdivided populations. Genet. Res. 70, 155-174. (doi:10.1017/S0016672397002954)
62. Lawniczak, M. K. N. et al. 2010 Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330, 512-514.(doi:10.1126/Science.1195755)
63. Kolaczkowski, B., Kern, A. D., Holloway, A. K. & Begun, D. J. 2011 Genomic differentiation between temperate and tropical Australian populations of Drosophila melanogaster. Genetics 187, 245-260. (doi:10.1534/Genetics.110.123059)
64. McGaugh, S. E. & Noor, M. A. F. 2012 Genomic impacts of chromosomal inversions in parapatric Drosophila species. Phil. Trans. R. Soc. B 367, 422-429.(doi:10.1098/rstb.2011.0250)
65. Strasburg, J. L., Scotti-Saintagne, C., Scotti, I., Lai, Z. & Rieseberg, L. H. 2009 Genomic patterns of adaptive divergence between chromosomally differentiated sunflower species. Mol. Biol. Evol. 26, 1341-1355. (doi:10.1093/Molbev/Msp043)
66. Neafsey, D. E. et al. 2010 SNP genotyping defines complex gene-flow boundaries among African malaria vector mosquitoes. Science 330, 514-517. (doi:10.1126/Science.1193036)
67. Beaumont, M. A. 2010 Approximate Bayesian computation in evolution and ecology. Annu. Rev. Ecol. Evol. Syst. 41, 379-406. (doi:10.1146/annurev-ecolsys-102209-144621)
68. Csillery, K., Blum, M. G. B., Gaggiotti, O. E. & Francois, O. 2010 Approximate Bayesian computation (ABC) in practice. Trends Ecol. Evol. 25, 410-418.(doi:10.1016/J.Tree.2010.04.001)