Comparative Molecular Population Genetics of the Xdh Locus in the Cactophilic Sibling Species Drosophila buzzatii and D. koepferae

Molecular Biology and Evolution

Volumn 21, Issue 1, 2004, Pages 141-152

  Piccinali, Romina ^a   Aguadé, Montserrat ^b   Hasson, Esteban ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Cactophilic Drosophila; Negative selection; Population expansion; Population structure; Xdh

Indexed keywords

ALLELE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; DNA SEQUENCE; DROSOPHILA; ELECTROPHORESIS; FEMALE; GENE; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC VARIABILITY; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POPULATION GENETICS; POPULATION STRUCTURE; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; XDH GENE;

AMINO ACID SEQUENCE; ANALYSIS OF VARIANCE; ANIMALS; ARGENTINA; BASE SEQUENCE; CACTACEAE; DNA PRIMERS; DROSOPHILA; EXONS; GENETICS, POPULATION; GEOGRAPHY; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS; VARIATION (GENETICS); XANTHINE DEHYDROGENASE;

ARACHNIDA; DROSOPHILA BUZZATII; DROSOPHILA KOEPFERAE; HEXAPODA;

EID: 1242306947     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msh006     Document Type: Article

References (87)

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. Andolfatto, P., F. Depaulis, and A. Navarro. 2001. Inversion polymorphisms and nucleotide variability in Drosophila. Genet. Res. Camb. 77:1-8.
3. Andolfatto, P., and M. Przeworski. 2000. A genome-wide departure from the standard neutral model in natural populations of Drosophila. Genetics 156:257-268.
4. Aquadro, C. F., K. M. Lado, and W. A. Noon. 1988. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting level of naturally occurring DNA restriction map variation and divergence. Genetics 119:875-888.
5. Begun, D. J., and P. Whitley. 2002. Molecular population genetics of Xdh and the evolution of base composition in Drosophila. Genetics 162:1725-1735.
6. 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.
7. Buchanon, B. A., and D. E. L. Johnson. 1983. Hidden electrophoretic variation at the xanthine dehydrogenase locus in a natural population of Drosophila melanogaster. Genetics 104:301-351.
8. Cabrera, A. 1976. Regiones Fitogeográficas de la Argentina. Enciclopedia Argentina de Agricultura y Ganadería. Facsículo 1. ACME, SACI, Buenos Aires.
9. Charlesworth, D., B. Charlesworth, and M. T. Morgan. 1995. The pattern of neutral molecular variation under the background selection model. Genetics 141:1619-1632.
10. Clark, A. G. 1997. Neutral behavior of shared polymorphism. Proc. Natl. Acad. Sci. USA 94:7730-7734.
11. Comeron, J. M., and M. Aguadé. 1996. Synonymous substitutions in the Xdh gene of Drosophila: heterogeneous distribution along the coding region. Genetics 144:1053-1062.
12. Coyne, J. A., S. Aulard, and A. Berry. 1991. Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics 129:791-802.
13. Coyne, J. A., W. Meyers, A. Crittenden, and P. Sniegowski. 1993. The fertility effects of pericentric inversiones in Drosophila melanogaster. Genetics 134:487-496.
14. Chovnic, A., W. Gelbart, and M. Mccarron. 1977. Organization of the rosy locus in Drosophila melanogaster. Cell 11:1-10.
15. De Brito, R. A., M. H. Manfrin, and F. M. Sene. 2002. Mitochondrial DNA phylogeography of Brazilian populations of Drosophila buzzatii. Genet. Mol. Biol. 25:161-171.
16. Durando, C. M., R. H. Baker, W. J. Etges, W. S. Breed, M. Wasserman, and R. Desalle. 2000. Phylogenetics analysis of the repleta species group of the genus Drosophila using multiple sources of characters. Mol. Phy. Evol. 16:296-307.
17. Etges, W. J. 1993. Genetics of host-cactus response and life-history evolution among ancestral and derived populations of cactophilic Drosophila mojavensis. Evolution 47:750-767.
18. Excoffier, L., P. E. Smouse, and J. M. Quattro. 1992. Analysis of the molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479-491.
19. Fanara, J. J., A. Fontdevila, and E. Hasson. 1999. Oviposition preference, viability, developmental time and body size in the cactophilic species Drosophila koepferae and D. buzzatii in association to their natural hosts. Evol. Ecol. 13:173-190.
20. Fanara, J. J., and E. Hasson. 2001. Oviposition acceptance and fecundity schedule in the cactophilic sibling species Drosophila buzzatii and D. koepferae on their natural hosts. Evolution 55:2615-2619.
21. Fay J. C., and C-I. Wu. 2000. Hitchhiking under positive darwinian selection. Genetics 155:1405-1413.
22. -. 2001. The neutral theory in the genomic era. Curr. Opin. Genet. Dev. 11:642-646.
23. Filatov, D. A., and D. Charlesworth. 1999. DNA polymorphism, haplotype structure and balancing selection in the Leavenworthia Pgi locus. Genetics 153:1423-1434.
24. Fontdevila, A., C. Pla, E. Hasson, M. Wasserman, A. Sanchez, H. Naveira, and A. Ruiz. 1988. Drosophila koepferae: a new member of the D. serido superspecies taxon. Ann. Entom. Soc. Am. 83:380-385.
25. Fu, Y-X., and W-H. Li. 1993. Statistical tests of neutrality of mutations. Genetics 133:693-709.
26. Galtier, N., F. Depaulis, and N. H. Barton. 2000. Detecting bottlenecks and selective sweeps from DNA sequence polymorphism. Genetics 155:981-987.
27. Gómez, G. A., and E. Hasson. 2003. Transpecific polymorphisms in an inversion linked esterase locus in Drosophila buzzatii. Mol. Biol. Evol. 20:410-423.
28. Hahn, M. W., M. D. Rausher, and C. W. Cunninham. 2002. Distinguishing between selection and population expansion in an experimental lineage of bacteriophage T7. Genetics 161:11-20.
29. Hartl, D. L., D. I. Nurmisnky, R. W. Jones, and E. R. Lozovskaya. 1994. Genome structure and evolution in Drosophila: applications of the framework P1 map. Proc. Natl. Acad. Sci. USA 91:6824-6829.
30. Hasson, E. 1988. Ecogenética evolutiva de Drosophila buzzatii y D. koepferae en las regiones áridas y semiáridas de la Argentina. PhD thesis. Universidad de Buenos Aires. Buenos Aires, Argentina.
31. Hasson, E., H. Naveira, and A. Fontdevila. 1992. The breeding sites of the Argentinian species of the Drosophila mulleri complex (subgenus Drosophila repleta group). Rev. Chilena de Hist. Nat. 65:319-326.
32. Hasson, E., C. Rodríguez, J. J. Fanara, H. Naveira, O. A. Reig, and A. Fontdevila. 1995. The evolutionary history of Drosophila buzzatii. XXVI. Macrogeographic patterns of inversion polymorphism in New World populations. J. Evol. Biol. 8:369-384.
33. Heed, W. B., and R. L. Mangan. 1986. Community ecology of the Sonoran Desert Drosophila. Pp. 311-345 in M. Ashburner, H. L. Carson, and J. N. Thompson Jr., eds. The genetics and biology of Drosophila, Vol. 3e. Academic Press, New York.
34. Higgins, D. G., J. D. Thompson, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
35. Hudson, R. R. 1990. Gene genealogies and the coalescent process. Oxf. Surv. Evol. Biol. 7:1-44.
36. -. 2000. A new statistic for detecting genetic differentiation. Genetics 155:2011-2014.
37. Hudson, R. R., D. D. Boos, and N. L. Kaplan. 1992. A statistical test for detecting geographical subdivision. Mol. Biol. Evol. 9:138-151.
38. Hudson, R. R., M. Kreitman, and M. Aguadé. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
39. Katz, L. A., and R. G. Harrison. 1997. Balancing selection on electrophoretic variation of phosphoglucose isomerase in two species of field cricket: Gyllus veletis and G. pennsylvanicus. Genetics 147:609-621.
40. Keith, T. P., L. D. Brooks, R. C. Lewontin, J. C. Martinez-Cruzado, and D. L. Rigby. 1985. Nearly identical allelic distributions of xanthine dehydrogenase in two populations of Drosophila pseudoobscura. Mol. Biol. Evol. 2:206-216.
41. Keith, T. P., M. A. Riley, M. Kreitman, R. C. Lewontin, D. Curtis, and G. Chambers. 1987. Sequence of the structural gene for xanthine dehydrogenase (rosy locus) in Drosophila melanogaster. Genetics 116:67-73.
42. Khadem, M., J. Rozas, C. Segarra, and M. Aguadé. 2001. DNA variation at the rp49 gene region in Drosophila madeirensis and D. subobscura from Madeira: inferences about the origin of an insular endemic species. J. Evol. Biol. 14:379-387.
43. 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.
44. Knibb, W. R., and J. S. F. Barker. 1988. Polymorphic inversion and esterase loci complex on chromosome 2 of Drosophila buzzatii II. Spatial variation. Aust. J. Biol. Sci. 41:239-246.
45. Kumar, S., K. Tamura, I. B. Jacobsen, and M. Nei. 2001. MEGA: molecular evolutionary genetics analysis. Version 2.01. http:// www.megasoftware.net.
46. Laayouni, H., E. Hasson, M. Santos, and A. Fontdevila. 2003. The evolutionary history of Drosophila buzzatii XXXV: inversion polymorphism and nucleotide variability in different regions of the second chromosome. Mol. Biol. Evol. 20:931-944.
47. Laayouni, H., M. Santos, and A. Fontdevila. 2000. Randomly amplified polymorphic DNA polymorphisms and sequence-tagged site landmarks. Genetics 156:1797-1816.
48. Laird, C. D. 1973. DNA of Drosophila chromosomes. Ann. Rev. Genet. 7:177-204.
49. 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.
50. Manfrin, M. H., R. O. A. De Brito, and F. M. Sene. 2001. Systematics and evolution of the Drosophila buzzatii (Diptera: Drosophilidae) cluster using mtDNA. Ann. Entomol. Soc. Am. 94:333-346.
51. McDonald, J. H., and M. Kreitman. 1991. Adaptative protein evolution at the Adh locus in Drosophila. Nature 351:652-654.
52. Navarro, A., E. Betrán, A. Barbadilla, and A. Ruiz. 1997. Recombination and gene flux caused by gene conversion and crossing over in inversion heterokaryotypes. Genetics 146:695-709.
53. Navarro-Sabaté, A., M. Aguadé, and C. Segarra. 1999. The relationship between allozyme and chromosomal polymorphism inferred from nucleotide variation at the Acph-1 gene region of Drosophila subobscura. Genetics 153:871-889.
54. Naveira, H., and A. Fontdevila. 1986. The evolutionary history of Drosophila buzzatii. XII. The genetic basis of sterility in hybrids between D. buzzatii and its sibling D. koepferae from Argentina. Genetics 114:841-857.
55. Pfeiler, E., and M. Markow. 2001. Ecology and population genetics of Sonoran Desert Drosophila. Mol. Ecol. 10:1787-1791.
56. Powell, J. R. 1997. Progress and prospects in evolutionary biology: the Drosophila model. Oxford University Press, New York.
57. Przeworski, M., B. Charlesworth, and J. D. Wall. 1999. Genealogies and weak purifying selection. Mol. Biol. Evol. 16:246-252.
58. Ptak S. E., and M. Pzeworski. 2002. Evidence for population growth in humans is confounded by fine-scale population structure. Trends Gen. 18:559-563.
59. Ramos-Onsins, S. E., and J. Rozas. 2002. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19:2092-2100.
60. Ramos-Onsins, S. E., B. E. Stranger, T. Mitchell-Olds, and M. Aguade. 2004. Mulitlocus analysis of variation and speciation in the closely related species Arabdopsis halleri and A. lyrata. Genetics (in press).
61. Ranz, J. M., C. Segarra, and A. Ruiz. 1997. Chromosomal homology and molecular organization of Muller's elements D and E in the Drosophila repleta species group. Genetics 145:281-295.
62. Riley, M. A., M. E. Hallas, and R. C. Lewontin. 1989. Distinguishing the forces controlling genetic variation at the Xdh locus in Drosophila pseudoobscura. Genetics 123:359-369.
63. Riley, M. A., S. R. Kaplan, and M. Veuille. 1992. Nucleotide polymorphism at the xanthine dehydrogenase locus in Drosophila pseudoobscura. Mol. Biol. Evol. 9:56-69.
64. Roberts, P. A., 1976. The genetics of chromosomal aberration. Pp. 67-184 in M. Ashburner and E. Novitski, eds. The genetics and biology of Drosophila, Vol. 1a. Academic Press, London.
65. Rodríguez, C., R. Piccinali, E. Levy, and E. Hasson. 2000. Contrasting population genetic structures using allozymes and the inversion polymorphism in Drosophila buzzatii. J. Evol. Biol. 13:976-984.
66. -. 2001. Gametic associations between inversion and allozyme polymorphisms in Drosophila buzzatii. J. Hered. 92:382-391.
67. Rodríguez-Trelles, F., L. Alarcón, and A. Fontdevila. 2000. Molecular evolution and phylogeny of the buzzatii complex (Drosophila repleta Group): a maximum-likelihood approach. Mol. Biol. Evol. 17:1112-1122.
68. Rodríguez-Trelles, F., R. Tarrío, and F. J. Ayala. 1999. Molecular evolution and phylogeny of the Drosophila saltans species group inferred from the Xdh gene. Mol. Phyl. Evol. 13:110-121.
69. -. 2000. Disparate evolution of paralogous introns in the Xdh gene of Drosophila. J. Mol. Evol. 50:123-130.
70. Rossi, M. S., E. Barrio, A. Latorre, J. E. Quezada-Díaz, E. Hasson, A. Moya, and A. Fontdevila. 1996. The evolutionary history of Drosophila buzzatii. XXX. Mitochondrial DNA polymorphism in original and colonized populations. Mol. Biol. Evol. 13:314-323.
71. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
72. Ruiz, A., and M. Wasserman. 1993. Evolutionary cytogenetics of the Drosophila buzzatii species complex. Heredity 70:582-596.
73. Sanchez, A. 1986. Relaciones Filogenéticas en los clusters martensis y buzzatii de Drosophila. PhD Thesis. Universidad Autónoma de Barcelona. Spain.
74. Schneider, S., D. Roessli, and L. Excoffier. 2000. Arlequín version 2.000: A software for population data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland. http://anthro.unige.ch/arlequin.
75. Shoemaker, D. D., and J. Jaenike. 1997. Habitat continuity and the genetic structure of Drosophila populations. Evolution 51:1326-1332.
76. Simonsen, K. L., G. A. Churchill, and C. F. Aquadro. 1995. Properties of statistical test of neutrality for DNA polymorphism data. Genetics 141:413-429.
77. Smirnova, I., M. T. Hamblin, C. Mcbride, B. Beutler, and A. Di Rienzo. 2001. Excess of rare amino acid polymorphisms in the toll-like receptor 4 in humans. Genetics 158:1657-1664.
78. Tajima, F. 1989. Statistical method for testing the neutral hypothesis by DNA polymorphism. Genetics 123:585-595.
79. Tarrío R., F. Rodríguez-Trelles, and F. J. Ayala. 1998. New Drosophila introns originate by duplication. Proc. Natl. Acad. Sci. USA 95:1658-1662.
80. Verrelli, B. C., and W. F. Eanes. 2000. Extensive amino acid polymorphism at the Pgm locus is consistent with adaptative evolution in D. melanogaster. Genetics 156:1737-1752.
81. Veuille, M., and L. M. King. 1995. Molecular basis of the polymorphism at the esterase-5B locus in Drosophila pseudoobscura. Genetics 141:255-262.
82. Wakeley, J. 2001. The coalescent in an island model of population subdivision with variation among demes. Theor. Popul. Biol. 59:133-144.
83. Wakeley, J., and N. Aliacar. 2001. Gene genealogies in a metapopulation. Genetics 159:893-905.
84. Wayne, M. L., and K. L. Simonsen. 1998. Statistical tests of neutrality in the age of weak selection. Trends Ecol. Evol. 13:236-240.
85. Weir, B. S. 1996. Genetic data analysis II. Sinauer Associates. Sunderland, Mass.
86. Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370.
87. Wooton, J. C., R. E. Nicolson, J. M. Cock, D. E. Walters, J. F. Burke, W. A. Doyle, and R. C. Bray. 1991. Enzymes depending on the pteridin molybdenum cofactor: sequence families, spectroscopic properties of molybdenum and possible cofactor-binding domains. Bioch. Biophys. Acta 1057:157-185.