Population transcriptomics of cactus host shifts in Drosophila mojavensis

Molecular Ecology

Volumn 21, Issue 10, 2012, Pages 2428-2439

  Matzkin, Luciano M ^a,b  

^a UNIVERSITY OF ALABAMA IN HUNTSVILLE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adaptation; cactophilic Drosophila; genotype by environment interactions; host shifts; transcriptional variation

Indexed keywords

TRANSCRIPTOME;

ANIMAL; ARTICLE; CACTACEAE; DNA MICROARRAY; DROSOPHILA; FEMALE; GENE; GENETICS; HOST RANGE; PHYSIOLOGY; POPULATION GENETICS;

ANIMALS; CACTACEAE; DROSOPHILA; FEMALE; GENES, INSECT; GENETICS, POPULATION; HOST SPECIFICITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTOME;

CACTACEAE; DROSOPHILA MELANOGASTER; DROSOPHILA MOJAVENSIS;

EID: 84860534714     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05549.x     Document Type: Article

References (91)

1. Abzhanov A, Kuo WP, Hartmann C, et al. (2006) The calmodulin pathway and evolution of elongated beak morphology in Darwin's finches. Nature, 442, 563-567. (Pubitemid 44167914)
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403-410.
3. Badyaev AV, (2009) Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the baldwin effect. Philosophical Transactions of the Royal Society B-Biological Sciences, 364, 1125-1141.
4. Baldwin JM, (1896) A new factor in evolution. American Naturalist, 30, 441-451, 536-553.
5. Bogwitz MR, Chung H, Magoc L, et al. (2005) Cyp12a4 confers lufenuron resistance in a natural population of Drosophila melanogaster. Proceedings of the National Academy of Sciences, USA, 102, 12807-12812. (Pubitemid 41279447)
6. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193. (Pubitemid 36181903)
7. Bono JM, Markow TA, (2009) Post-zygotic isolation in cactophilic Drosophila: larval viability and adult life-history traits of D. mojavensis/D. arizonae hybrids. Journal of Evolutionary Biology, 22, 1387-1395.
8. Chung H, Sztal T, Pasricha S, et al. (2009) Characterization of Drosophila melanogaster cytochrome P450 genes. Proceedings of the National Academy of Sciences, USA, 106, 5731-5736.
9. Consortium DG, (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature, 450, 203-218.
10. Daborn P, Boundy S, Yen J, Pittendrigh B, ffrench-Constant R, (2001) DDT resistance in Drosophila correlates with cyp6g1 over-expression and confers cross-resistance to the neonicotinoid imidacloprid. Molecular Genetics and Genomics, 266, 556-563. (Pubitemid 33145117)
11. Daborn PJ, Yen JL, Bogwitz MR, et al. (2002) A single P450 allele associated with insecticide resistance in Drosophila. Science, 297, 2253-2256.
12. Daborn PJ, Lumb C, Boey A, et al. (2007) Evaluating the insecticide resistance potential of eight Drosophila melanogaster cytochrome P450 genes by transgenic over-expression. Insect Biochemistry and Molecular Biology, 37, 512-519. (Pubitemid 46602982)
13. Danielson P, MacIntyre R, Fogleman J, (1997) Molecular cloning of a family of xenobiotic-inducible drosophilid cytochrome p450s: evidence for involvement in host-plant allelochemical resistance. Proceedings of the National Academy of Sciences, USA, 94, 10797-10802. (Pubitemid 27430814)
14. Danielson PB, Foster JLM, McMahill MM, Smith MK, Fogleman JC, (1998) Induction by alkaloids and phenobarbital of family 4 cytochrome p450s in Drosophila: evidence for involvement in host plant utilization. Molecular and General Genetics, 259, 54-59. (Pubitemid 28409816)
15. Dennis G, Sherman BT, Hosack DA, et al. (2003) David: database for annotation, visualization, and integrated discovery. Genome Biology, 4, R60.
16. Dworkin I, Jones CD, (2009) Genetic changes accompanying the evolution of host specialization in Drosophila sechellia. Genetics, 181, 721-736.
17. Etges WJ, (1989) Evolution of developmental homeostasis in Drosophila mojavensis. Evolutionary Ecology, 3, 189-201. (Pubitemid 20423273)
18. Etges WJ, (1990) Direction of life history evolution in Drosophila mojavensis. In: Ecological and Evolutionary Genetics of Drosophila (eds, Barker JSF, Starmer WT, and, MacIntyre RJ,), pp. 37-56. Plenum Press, New York, NY.
19. Etges WJ, Heed WB, (1987) Sensitivity to larval density in populations of Drosophila mojavensis: influences of host plant variation on components fitness. Oecologia, 71, 375-381.
20. Feder ME, Mitchell-Olds T, (2003) Evolutionary and ecological functional genomics. Nature Review Genetics, 4, 649-655.
21. Fellows DF, Heed WB, (1972) Factors affecting host plant selection in desert-adapted cactiphilic Drosophila. Ecology, 53, 850-858.
22. Festucci-Buselli RA, Carvalho-Dias AS, de Oliveira-Andrade M, et al. (2005) Expression of cyp6g1 and cyp12d1 in DDT resistant and susceptible strains of Drosophila melanogaster. Insect Molecular Biology, 14, 69-77. (Pubitemid 40218085)
23. Feyereisen R, (2005) Insect cytochrome P450. In: Comprehensive Molecular Insect Science (eds, Gilbert LI, Iatrou K, and, Gill SS,), pp. 1-77. Elsevier, Amsterdam.
24. Fogleman JC, Abril JR, (1990) Ecological and evolutionary importance of host plant chemistry. In: Ecological and Evolutionary Genetics of Drosophila (eds, Barker JSF, Starmer WT, and, MacIntyre RJ,), pp. 121-143. Plenum Press, New York, NY.
25. Fogleman JC, Starmer WT, (1985) Analysis of the community structure of yeasts associated with the decaying stems of cactus. III. Stenocereus thurberi. Microbial Ecology, 11, 165-173.
26. Fogleman JC, Starmer WT, Heed WB, (1981) Larval selectivity for yeast species by Drosophila mojavensis in natural substrates. Proceedings of the National Academy of Sciences, USA, 78, 4435-4439.
27. Gilad Y, Rifkin SA, Bertone P, Gerstein M, White KP, (2005) Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. Genome Research, 15, 674-680. (Pubitemid 41043637)
28. Guo S, Kim J, (2007) Molecular evolution of Drosophila odorant receptor genes. Molecular Biology and Evolution, 24, 1198-1207. (Pubitemid 47343644)
29. Hahn MW, Han MV, Han S-G, (2007) Gene family evolution across 12 Drosophila genomes. Plos Genetics, 3, e197.
30. Heed WB, (1978) Ecology and genetics of Sonoran desert Drosophila. In: Ecological Genetics: The interface (ed, Brussard PF,), pp. 109-126. Springer-Verlag, New York.
31. Heed WB, (1982) The origin of Drosophila in the sonoran desert. In: Ecological Genetics and Evolution: The Cactus-yeast-Drosophila Model System (eds, Barker JSF, and, Starmer WT,), pp. 65-80. Academic Press, New York.
32. Hosack DA, Dennis G, Sherman BT, Lane HC, Lempicki RA, (2003) Identifying biological themes within lists of genes with ease. Genome Biology, 4, R70.
33. Irizarry RA, Hobbs B, Collin F, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
34. Johnson WR, (1980) Chromosomal Polymorphism in Natural Populations of the Desert Adapted Species, Drosophila mojavensis. University of Arizona, Tucson, AZ.
35. Kelleher ES, Swanson WJ, Markow TA, (2007) Gene duplication and adaptive evolution of digestive proteases in Drosophila arizonae female reproductive tracts. Plos Genetics, 3, 1541-1549. (Pubitemid 47358089)
36. King M-C, Wilson AC, (1975) Evolution at two levels in humans and chimpanzees. Science, 188, 107-116.
37. Kircher HW, (1982) Chemical composition of cacti and its relationship to Sonoran desert Drosophila. In: Ecological Genetics and Evolution: The Cactus-yeast-Drosophila Model System (eds, Barker JSF, and, Starmer WT,), pp. 143-158. Academic Press, New York.
38. Le Goff G, Hilliou F, Siegfried BD, et al. (2006) Xenobiotic response in Drosophila melanogaster: sex dependence of P450 and gst gene induction. Insect Biochemistry and Molecular Biology, 36, 674-682. (Pubitemid 44108644)
39. Li HM, Buczkowski G, Mittapalli O, et al. (2008) Transcriptomic profiles of Drosophila melanogaster third instar larval midgut and responses to oxidative stress. Insect Molecular Biology, 17, 325-339.
40. Lofdahl KL, (1985) A Quantitative Genetic Analysis of Habitat Selection Behavior in the Cactus-breeding Species Drosophila mojavensis. Ph.D. Thesis, University of Chicago, Chicago.
41. Low WY, Ng HL, Morton CJ, et al. (2007) Molecular evolution of glutathione s-transferases in the genus Drosophila. Genetics, 177, 1363-1375. (Pubitemid 350277038)
42. Lumjuan N, McCarroll L, Prapanthadara LA, Hemingway J, Ranson H, (2005) Elevated activity of an epsilon class glutathione transferase confers DDT resistance in the dengue vector, Aedes aegypti. Insect Biochemistry and Molecular Biology, 35, 861-871. (Pubitemid 41556949)
43. Luque T, O'Reilly DR, (2002) Functional and phylogenetic analyses of a putative Drosophila melanogaster UDP-glycosyltransferase gene. Insect Biochemistry and Molecular Biology, 32, 1597-1604. (Pubitemid 35368808)
44. Machado CA, Matzkin LM, Reed LK, Markow TA, (2007) Multilocus nuclear sequences reveal intra- and interspecific relationships among chromosomally polymorphic species of cactophilic Drosophila. Molecular Ecology, 16, 3009-3024. (Pubitemid 47035465)
45. Matzkin LM, (2004) Population genetics and geographic variation of alcohol dehydrogenase (Adh) paralogs and glucose-6-phosphate dehydrogenase (G6pd) in Drosophila mojavensis. Molecular Biology and Evolution, 21, 276-285. (Pubitemid 38314616)
46. Matzkin LM, (2005) Activity variation in alcohol dehydrogenase paralogs is associated with adaptation to cactus host use in cactophilic. Drosophila Molecular Ecology, 14, 2223-2231. (Pubitemid 40772434)
47. Matzkin LM, (2008) The molecular basis of host adaptation in cactophilic Drosophila: molecular evolution of a glutathione s-transferase gene (GstD1) in Drosophila mojavensis. Genetics, 178, 1073-1083. (Pubitemid 351398814)
48. Matzkin LM, Watts TD, Bitler BG, Machado CA, Markow TA, (2006) Functional genomics of cactus host shifts in Drosophila mojavensis. Molecular Ecology, 15, 4635-4643. (Pubitemid 44749575)
49. McBride CS, (2007) Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proceedings of the National Academy of Sciences, USA, 104, 4996-5001. (Pubitemid 47186165)
50. Meyer E, Aglyamova GV, Matz MV, (2011) Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-seq procedure. Molecular Ecology, 20, 3599-3616.
51. Nuzhdin S, Wayne M, Harmon K, McIntyre L, (2004) Common pattern of evolution of gene expression level and protein sequence in Drosophila. Molecular Biology and Evolution, 21, 1308-1317. (Pubitemid 38823733)
52. Ohta T, (1992) The nearly neutral theory of molecular evolution. Annual Review of Ecology and Systematics, 23, 263-286. (Pubitemid 24412250)
53. Pedra JHF, McIntyre LM, Scharf ME, Pittendrigh BR, (2004) Genome wide transcription profile of field- and laboratory-selected dichlorodiphenyltrichloroethane (DDT)-resistant Drosophila. Proceedings of the National Academy of Sciences, USA, 101, 7034-7039. (Pubitemid 38596438)
54. Pfeiler E, Castrezana S, Reed LK, (2009) Genetic, ecological and morphological differences among populations of the cactophilic Drosophila mojavensis from southwestern USA and northwestern Mexico, with descriptions of two new subspecies. Journal of Natural History, 43, 923-938.
55. Pigliucci M, Murren CJ, (2003) Perspective: genetic assimilation and a possible evolutionary paradox: can macroevolution sometimes be so fast as to pass us by? Evolution, 57, 1455-1464. (Pubitemid 36953635)
56. Pyke FM, Bogwitz MR, Perry T, et al. (2004) The genetic basis of resistance to diazinon in natural populations of Drosophila melanogaster. Genetica, 121, 13-24. (Pubitemid 38448428)
57. Ranson H, Hemingway J, (2005) Glutathione transferases. In: Comprehensive Molecular Insect Science (eds, Gilbert LI, Iatrou K, and, Gill SS,), pp. 383-402. Elsevier, Amsterdam, the Netherland.
58. Ranson H, Rossiter L, Ortelli F, et al. (2001) Identification of a novel class of insect glutathione s-transferases involved in resistance to DDT in the malaria vector Anopheles gambiae. Biochemical Journal, 359, 295-304. (Pubitemid 32999773)
59. Reed LK, Nyboer M, Markow TA, (2007) Evolutionary relationships of Drosophila mojavensis geographic host races and their sister species Drosophila arizonae. Molecular Ecology, 16, 1007-1022.
60. Rifkin SA, Kim J, White KP, (2003) Evolution of gene expression in the Drosophila melanogaster subgroup. Nature Genetics, 33, 138-144. (Pubitemid 36177064)
61. Ruiz A, Heed WB, (1988) Host-plant specificity in the cactophilic Drosophila mulleri species complex. Journal of Animal Ecology, 57, 237-249. (Pubitemid 19317709)
62. Ruiz A, Heed WB, Wasserman M, (1990) Evolution of the mojavensis cluster of cactophilic Drosophila with descriptions of two new species. Journal of Heredity, 81, 30-42. (Pubitemid 20182438)
63. Sambandan D, Carbone MA, Anholt RRH, Mackay TEC, (2008) Phenotypic plasticity and genotype by environment interaction for olfactory behavior in Drosophila melanogaster. Genetics, 179, 1079-1088.
64. Shapiro MD, Marks ME, Peichel CL, et al. (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature, 428, 717-723. (Pubitemid 38508276)
65. Starmer WT, (1982a) Analysis of the community structure of yeasts associated with the decaying stems of cactus. I. Stenocereus gummosus. Microbial Ecology, 8, 71-81.
66. Starmer WT, (1982b) Associations and interactions among yeasts, Drosophila and their habitats. In: Ecological Genetics and Evolution: The Cactus-yeast-Drosophila Model System (eds, Barker JSF, and, Starmer WT,), pp. 159-174. Academic Press, New York, NY.
67. Starmer WT, Gilbert DG, (1982) A quick and reliable method for sterilizing eggs. Drosophila Information Service, 58, 170-171.
68. Starmer WT, Heed WB, Rockwood-Sluss ES, (1977) Extension of longevity in Drosophila mojavensis by environmental ethanol: differences between subraces. Proceedings of the National Academy of Sciences, USA, 74, 387-391.
69. Starmer WT, Lachance MA, Phaff HJ, Heed WB, (1990) The biogeography of yeasts associated with decaying cactus tissue in North America, the Caribbean, and northern Venezuela. In: Evolutionary Biology (eds, Hecht MK, Wallace B, and, Macintyre RJ,), pp. 253-296. Plenum Publishing Corporation, New York.
70. Stone J, Wray G, (2001) Rapid evolution of cis-regulatory sequences via local point mutations. Molecular Biology and Evolution, 18, 1764-1770. (Pubitemid 32776927)
71. Storey J, Tibshirani R, (2003) Statistical significance for genomewide studies. Proccedings of the National Academy of Sciences, USA, 100, 9440-9445. (Pubitemid 37033947)
72. Sun W, Margam VM, Sun L, et al. (2006) Genome-wide analysis of phenobarbital-inducible genes in Drosophila melanogaster. Insect Molecular Biology, 15, 455-464. (Pubitemid 44166567)
73. Telonis-Scott M, Hallas R, McKechnie SW, Wee CW, Hoffmann AA, (2009) Selection for cold resistance alters gene transcript levels in Drosophila melanogaster. Journal of Insect Physiology, 55, 549-555.
74. Theopold U, Rissler M, Fabbri M, Schmidt O, Natori S, (1999) Insect glycobiology: a lectin multigene family in Drosophila melanogaster. Biochemical and Biophysical Research Communications, 261, 923-927. (Pubitemid 29408158)
75. Tijet N, Helvig C, Feyereisen R, (2001) The cytochrome P450 gene superfamily in Drosophila melanogaster: annotation, intron-exon organization and phylogeny. Gene, 262, 189-198. (Pubitemid 32155349)
76. Tweedie S, Ashburner M, Falls K, et al. (2009) FlyBase: enhancing Drosophila gene ontology annotations. Nucleic Acids Research, 37, D555-D559.
77. Vacek DC, (1979) The Microbial Ecology of the Host Plants of Drosophila mojavensis. Ph.D. Thesis, University of Arizona, Tucson, AZ.
78. Vosshall LB, Stocker RE, (2007) Molecular architecture of smell and taste in Drosophila. Annual Review of Neuroscience, 30, 505-533. (Pubitemid 47218766)
79. Waddington CH, (1953) Genetic assimilation of an acquired character. Evolution, 7, 118-126.
80. Wang Q, Hasan G, Pikielny CW, (1999) Preferential expression of biotransformation enzymes in the olfactory organs of Drosophila melanogaster, the antennae. Journal of Biological Chemistry, 274, 10309-10315.
81. Wasserman M, (1982) Evolution in the repleta group. In: The Genetics and Biology of Drosophila (eds, Ashburner M, Carson HL, and, Thompson JN,), pp. 61-139. Academic Press, London.
82. Werner T, Koshikawa S, Williams TM, Carroll SB, (2010) Generation of a novel wing colour pattern by the Wingless morphogen. Nature, 464, 1143-1148.
83. West-Eberhard MJ, (2003) Developmental Plasticity and Evolution. Oxford University Press, New York.
84. West-Eberhard MJ, (2005) Phenotypic accommodation: adaptive innovation due to developmental plasticity. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution, 304B, 610-618. (Pubitemid 43266578)
85. Whitehead A, Crawford DL, (2006) Neutral and adaptive variation in gene expression. Proceedings of the National Academy of Sciences, USA, 103, 5425-5430.
86. Williams LM, Oleksiak MF, (2011) Evolutionary and functional analyses of cytochrome P4501A promoter polymorphisms in natural populations. Molecular Ecology, 20, 5236-5247.
87. Willoughby L, Chung H, Lumb C, et al. (2006) A comparison of Drosophila melanogaster detoxification gene induction responses for six insecticides, caffeine and phenobarbital. Insect Biochemistry and Molecular Biology, 36, 934-942. (Pubitemid 46053796)
88. Wittkopp PJ, Haerum BK, Clark AG, (2004) Evolutionary changes in cis and trans gene regulation. Nature, 430, 85-88. (Pubitemid 38915229)
89. Wittkopp PJ, Haerum BK, Clark AG, (2008) Regulatory changes underlying expression differences within and between Drosophila species. Nature Genetics, 40, 346-350. (Pubitemid 351311764)
90. Wolfinger RD, Gibson G, Wolfinger ED, et al. (2001) Assessing gene significance from cDNA microarray expression data via mixed models. Journal of Computational Biology, 8, 625-637. (Pubitemid 34053500)
91. Wray GA, Hahn MW, Abouheif E, et al. (2003) The evolution of transcriptional regulation in eukaryotes. Molecular Biology and Evolution, 20, 1377-1419. (Pubitemid 37086669)