Incompatibility and competitive exclusion of genomic segments between sibling Drosophila species

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Fang, Shu ^a   Yukilevich, Roman ^b,c   Chen, Ying ^b,d   Turissini, David A ^b   Zeng, Kai ^b,e,g   Boussy, Ian A ^d   Wu, Chung I ^b,e,f  

^a BIODIVERSITY RESEARCH CENTER   (Taiwan)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNION COLLEGE   (United States)

^d LOYOLA UNIVERSITY CHICAGO   (United States)

^e SUN YAT SEN UNIVERSITY   (China)

^f Chinese Academy of Sciences   (China)

^g UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; COMPETITIVE BEHAVIOR; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA SECHELLIA; DROSOPHILA SIMULANS; FEMALE; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC INCOMPATIBILITY; GENETIC LINE; GENOME ANALYSIS; INSECT GENOME; INTRASPECIFIC COMPETITION; INTROGRESSION; MALE; MATING SUCCESS; MOLECULAR DYNAMICS; NONHUMAN; REPRODUCTIVE FITNESS; SPECIES DIFFERENTIATION; WILD TYPE; ALLELE; ANIMAL; CHROMOSOME MAP; GENETIC SELECTION; GENETICS; GENOME; HYBRIDIZATION; INFERTILITY; REPRODUCTIVE ISOLATION; SPECIES DIFFERENCE;

DROSOPHILA SECHELLIA; DROSOPHILA SIMULANS;

ALLELES; ANIMALS; CHROMOSOME MAPPING; DROSOPHILA; GENETIC FITNESS; GENETIC SPECIATION; GENOME, INSECT; HYBRIDIZATION, GENETIC; INFERTILITY; REPRODUCTIVE ISOLATION; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 84864063116     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002795     Document Type: Article

References (56)

1. Dobzhansky T, (1937) Genetics and the origin of species New York Columbia University Press.
2. Mayr E, (1959) Where are we? Cold Spring Harbor Symp Quant Biol 24: 1-14.
3. Mayr E, (1963) Animal species and evolution Cambridge Belknap Press.
4. Mayr E, (1954) Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford EB, editors. Evolution as a process London Allen & Unwin pp. 157-180.
5. Coyne J, Orr A, (2004) Speciation Sunderland Sinauer Associates, Inc.
6. Wu CI, (2001) The genic view of the process of speciation. J Evol Biol 14: 851-865.
7. Barton NH, (2008) The effect of a barrier to gene flow on patterns of geographic variation. Genet Res 90: 139-149.
8. Via S, (2009) Natural selection in action during speciation. Proc Natl Acad Sci USA 106: 9939-9946.
9. Turner TL, Hahn MW, Nuzhdin SV, (2005) Genomic islands of speciation in Anopheles gambiae. PLoS Biol 3: e285 doi:10.1371/journal.pbio.0030285.
10. Harr B, (2006) Genomic islands of differentiation between house mouse subspecies. Genome Res 16: 730-737.
11. Yatabe Y, Kane NC, Scotti-Saintagne C, Rieseberg LH, (2007) Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris. Genetics 175: 1883-1893.
12. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic divergence. Mol Ecol 18: 375-402.
13. Butlin RK, (2010) Population genomics and speciation. Genetica 138: 409-418.
14. Feder JL, Nosil P, (2010) The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation. Evolution 64: 1729-1747.
15. Michel AP, Sim S, Powell TH, Taylor MS, Nosil P, et al. (2010) Widespread genomic divergence during sympatric speciation. Proc Natl Acad Sci USA 107: 9724-9729.
16. Lawniczak MKN, Emrich SJ, Holloway AK, Regier AP, Olson M, et al. (2010) Widespread divergence between incipient Anopheles gambiae species revealed by whole genome sequences. Science 330: 512-514.
17. Yukilevich R, Turner TL, Aoki F, Nuzhdin SV, True JR, (2010) Patterns and processes of genome-wide divergence between North American and African Drosophila melanogaster. Genetics 186: 219-239.
18. Wu CI, Palopoli MF, (1994) Genetics of postmating reproductive isolation in animals. Annu Rev Genet 28: 283-308.
19. True JR, Weir BS, Laurie CC, (1996) A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142: 819-837.
20. Naveira H, Maside X, (1998) The genetics of hybrid male sterility in Drosophila. In: Howard DJ, Berlocher SH, editors. Endless forms: species and speciation Oxford Oxford University Press pp. 330-338.
21. Tao Y, Chen S, Hartl DL, Laurie CC, (2003) Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164: 1383-1397.
22. Presgraves DC, (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955-972.
23. Masly JP, Presgraves DC, (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5: e243 doi:10.1371/journal.pbio.0050243.
24. Ting CT, Tsaur SC, Wu ML, Wu CI, (1998) A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501-1504.
25. Wittbrodt J, Adam D, Malitschek B, Maueler W, Raulf F, et al. (1989) Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341: 415-421.
26. Barbash DA, Siino DF, Tarone AM, Roote J, (2003) A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc Natl Acad Sci USA 100: 5302-5307.
27. Barbash DA, Awadalla P, Tarone AM, (2004) Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol 2: e142 doi:10.1371/journal.pbio.0020142.
28. Presgraves DC, Balagopalan L, Abmayr SM, Orr HA, (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715-719.
29. 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.
30. Masly JP, Jones CD, Noor MA, Locke J, Orr HA, (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448-1450.
31. Phadnis N, Orr HA, (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376-379.
32. Johnson NA, (2010) Hybrid incompatibility genes: remnants of a genomic battlefield? Trends Genet 26: 317-325.
33. Barton NH, Gale KS, (1993) Genetic analysis of hybrid zones. In: Harrison RG, editors. Hybrid zones and the evolutionary process Oxford Oxford University Press pp. 13-45.
34. Mercer KL, Wyse DL, Shaw RG, (2006) Effects of competition on fitness of wild and crop-wild hybrid sunflower from a diversity of wild populations and crop lines. Evolution 60: 2044-2055.
35. Barton NH, Hewitt GM, (1981) Hybrid zones and speciation. In: Atchley WR, Woodruff D, editors. Evolution and Speciation Cambridge Cambridge University Press pp. 109-145.
36. 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.
37. McDermott SR, Kliman RM, (2008) Estimation of isolation times of the island species in the Drosophila simulans complex from multilocus DNA sequence data. PLoS ONE 3: e2442 doi:10.1371/journal.pone.0002442.
38. Lachaise D, David JR, Lemeunier F, Tsacas L, Ashburner M, (1986) The reproductive relationships of Drosophila sechellia with D. mauritiana, D. simulans, and D. melanogaster from the Afrotropical region. Evolution 40: 262-271.
39. Lachaise D, Cariou ML, David JR, Lemeunier F, Tsacas L, et al. (1988) Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol 22: 159-225.
40. Lachaise D, Silvain JF, (2004) How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120: 17-39.
41. Haldane JBS, (1924) A mathematical theory of natural and artificial selection, Part I. Trans Camb Philos Soc 23: 19-41.
42. Sharp PM, (1984) The effect of Inbreeding on competitive male-mating ability in Drosophila melanogaster. Genetics 106: 601-612.
43. Spencer LJ, Snow AA, (2001) Fecundity of transgenic wild-crop hybrids of Cucurbita pepo (Cucurbitaceae): implications for crop-to-wild gene flow. Heredity 86: 694-702.
44. Stewart CN Jr, Halfhill MD, Warwick SI, (2003) Transgene introgression from genetically modified crops to their wild relatives. Nat Rev Gen 4: 806-817.
45. Song ZP, Lu BR, Wang B, Chen JK, (2004) Fitness estimation through performance comparison of F1 hybrids with their parental species Oryza rufipogon and O. sativa. Ann Bot 93: 311-316.
46. Wright S, (1932) The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proc Sixth Inter Congr Genet 1: 356-366.
47. Gavrilets S, (2004) Fitness landscapes and the origin of species Princeton Princeton University Press.
48. Carter AJ, Hermisson J, Hansen TF, (2005) The role of epistatic gene interactions in the response to selection and the evolution of evolvability. Theor Popul Biol 68: 179-196.
49. Orr HA, (2006) The population genetics of adaptation on correlated fitness landscapes: the block model. Evolution 60: 1113-1124.
50. Yukilevich R, Lachance J, Aoki F, True JR, (2008) Long-term adaptation of epistatic genetic networks. Evolution 62: 2215-2235.
51. Gavrilets S, (2000) Waiting time to parapatric speciation. Proc Biol Sci 267: 2483-2492.
52. Wade MJ, (2002) A gene's view of epistasis, selection and speciation. J Evol Biol 15: 337-346.
53. Macdonald SJ, Goldstein DB, (1999) A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153: 1683-1699.
54. Colson I, MacDonald SJ, Goldstein DB, (1999) Microsatellite markers for interspecific mapping of Drosophila simulans and D. sechellia. Mol Ecol 8: 1951-1955.
55. Wu CI, Hollocher H, Begun DJ, Aquadro CF, Xu Y, et al. (1995) Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci USA 92: 2519-2523.
56. Casares P, Carracedo MC, Rio BD, Piñeiro R, García-Flórez L, et al. (1998) Disentangling the effects of mating propensity and mating choice in Drosophila. Evolution 52: 126-133.