Signatures of selection in the Iberian honey bee (Apis mellifera iberiensis) revealed by a genome scan analysis of single nucleotide polymorphisms

Molecular Ecology

Volumn 22, Issue 23, 2013, Pages 5890-5907

  Chávez Galarza, Julio ^a   Henriques, Dora ^a   Johnston, J Spencer ^b   Azevedo, João C ^a   Patton, John C ^c   Muñoz, Irene ^d   De La Rúa, Pilar ^d   Pinto, M Alice ^a  

^a INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Purdue University ^*  (United States)

^d UNIVERSITY OF MURCIA   (Spain)

Author keywords

Apis mellifera iberiensis; balancing selection; directional selection; F ST outlier tests; genome scan; single nucleotide polymorphism

Indexed keywords

APIS MELLIFERA; APIS MELLIFERA IBERIENSIS;

ANIMAL; APIS MELLIFERA IBERIENSIS; ARTICLE; BALANCING SELECTION; BEE; BIOLOGICAL MODEL; DIRECTIONAL SELECTION; FST OUTLIER TESTS; GENE LOCUS; GENETIC SELECTION; GENETICS; GENOME; GENOME SCAN; MALE; POPULATION GENETICS; PORTUGAL; SINGLE NUCLEOTIDE POLYMORPHISM; SPAIN;

APIS MELLIFERA IBERIENSIS; BALANCING SELECTION; DIRECTIONAL SELECTION; FST OUTLIER TESTS; GENOME SCAN; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; BEES; GENETIC LOCI; GENETICS, POPULATION; GENOME; MALE; MODELS, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; PORTUGAL; SELECTION, GENETIC; SPAIN;

EID: 84888640715     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12537     Document Type: Article

References (128)

1. Ai H, Huang L, Ren J, (2013) Genetic diversity, linkage disequilibrium and selection signatures in chinese and Western pigs revealed by genome-wide SNP markers. PLoS One, 8, e56001.
2. Allendorf FW, Luikart G, (2007) Conservation and the Genetics of Populations, 1st edn. Blackwell Publishing, Malden.
3. ST-outlier method. BMC Bioinformatics, 9, 323.
4. Arias MC, Rinderer TE, Sheppard WS, (2006) Further characterization of honey bees from the Iberian Peninsula by allozyme, morphometric and mtDNA haplotype analyses. Journal of Apicultural Research, 45, 188-196.
5. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980.
6. Beaumont MA, Nichols RA, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London, Series B: Biological Sciences, 263, 1619-1626.
7. Behura SK, Severson DW, (2012) Comparative analysis of codon usage bias and codon context patterns between dipteran and hymenopteran sequenced genomes. PLoS One, 7, e43111.
8. Belyaeva OV, Lee SA, Kolupaev OV, Kedishvili NY, (2009) Identification and characterization of retinoid-active short-chain dehydrogenases/reductases in Drosophila melanogaster. Biochimica et Biophysica Acta-General Subjects, 1790, 1266-1273.
9. Beye M, Gattermeier I, Hasselmann M, et al,. (2006) Exceptionally high levels of recombination across the honey bee genome. Genome Research, 16, 1339-1344.
10. Blacquière T, Smagghe G, van Gestel CAM, Mommaerts V, (2012) Neonicotinoids in bees: A review on concentrations, side-effects and risk assessment. Ecotoxicology, 21, 1581.
11. Bonin A, Taberlet P, Miaud C, Pompanon F, (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Molecular Biology and Evolution, 23, 773-783.
12. Buchon N, Broderick NA, Poidevin M, Pradervand S, Lemaitre B, (2009) Drosophila intestinal response to bacterial infection: Activation of host defense and stem cell proliferation. Cell Host & Microbe, 5, 200-211.
13. Buckley J, Butlin RK, Bridle JR, (2012) Evidence for evolutionary change associated with the recent range expansion of the British butterfly, Aricia agestis, in response to climate change. Molecular Ecology, 21, 267-280.
14. Bull DL, Whitten CJ, (1972) Factors influencing organophosphorus insecticide resistance in tobacco budworms. Journal of Agricultural and Food Chemistry, 20, 561-564.
15. Bull JC, Ryabov EV, Prince G, et al,. (2012) A strong immune response in young adult honey bees masks their increased susceptibility to infection compared to older bees. PLoS Pathogens, 8, e1003083.
16. Bunce JA, Isbell LA, Neitz M, et al,. (2011) Characterization of opsin gene alleles affecting color vision in a wild population of titi monkeys (Callicebus brunneus). American Journal of Primatology, 73, 189-196.
17. Burrill RM, Dietz A, (1981) The response of honey bees to variations in solar radiation and temperature. Apidologie, 12, 319-328.
18. Cafferty P, Yu L, Long H, Rao Y, (2006) Semaphorin-1a functions as a guidance receptor in the Drosophila visual system. Journal of Neuroscience, 26, 3999-4003.
19. Camps M, Herman A, Loh E, Loeb LA, (2007) Genetic constraints on protein evolution. Critical Reviews in Biochemistry and Molecular Biology, 42, 313-326.
20. Cánovas F, De la Rúa P, Serrano J, Galián J, (2008) Geographical patterns of mitochondrial DNA variation in Apis mellifera iberiensis (Hymenoptera: Apidae). Journal of Zoological Systematics and Evolutionary Research, 46, 24-30.
21. Cánovas F, De la Rúa P, Serrano J, Galián J, (2011) Microsatellite variability reveals beekeeping influences on Iberian honey bee populations. Apidologie, 42, 235-251.
22. Claudianos C, Ranson H, Johnson RM, et al,. (2006) A deficit of detoxification enzymes: Pesticide sensitivity and environmental response in the honey bee. Insect Molecular Biology, 15, 615-636.
23. Cooke GM, Chao NL, Beheregaray LB, (2012) Divergent natural selection with gene flow along major environmental gradients in Amazonia: Insights from genome scans, population genetics and phylogeography of the characin fish Triportheus albus. Molecular Ecology, 21, 2410-2427.
24. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411-1423.
25. Cornuet JM, Fresnaye J, (1989) Biometrical study of honey bee populations from Spain and Portugal. Apidologie, 20, 93-101.
26. Cox-Foster DL, Conlan S, Holmes EC, et al,. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science, 318, 283-287.
27. De Jong MA, Collins S, Beldade P, Brakefield PM, Zwaan BJ, (2013) Footprints of selection in wild populations of Bicyclus anynana along a latitudinal cline. Molecular Ecology, 22, 341-353.
28. Dietemann V, Pirk CWW, Crewe R, (2009) Is there a need for conservation of honey bees in Africa? Apidologie, 40, 285-295.
29. Dussaubat C, Brunet JL, Higes M, et al,. (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One, 7, e37017.
30. Earl JB, Britt SG, (2006) Expression of Drosophila rhodopsins during photoreceptor cell differentiation: Insights into R7 and R8 cell subtype commitment. Gene Expression Patterns, 6, 687-694.
31. Engel MS, (1999) The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae; Apis). Journal of Hymenoptera Research, 8, 165-196.
32. vanEngelsdorp D, Meixner MD, (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology, 103, S80-S95.
33. vanEngelsdorp D, Evans JD, Saegerman C, et al,. (2009) Colony collapse disorder: A descriptive study. PLoS One, 4, e6481.
34. Evans JD, (2006) Beepath: An ordered quantitative-PCR array for exploring honey bee immunity and disease. Journal of Invertebrate Pathology, 93, 135-139.
35. Evans JD, Spivak M, (2010) Socialized medicine: Individual and communal disease barriers in honey bees. Journal of Invertebrate Pathology, 103, S62-S72.
36. Excoffier L, Lischer HE, (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
37. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity (Edinb), 103, 285-298.
38. Feyereisen R, (1999) Insect P450 Enzymes. Annual Review of Entomology, 44, 507-533.
39. Ffrench-Constant RH, Daborn PJ, Le Goff G, (2004) The genetics and genomics of insecticide resistance. Trends in Genetics, 20, 163-170.
40. Foll M, Gaggiotti O, (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics, 174, 875-891.
41. Foll M, Gaggiotti O, (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics, 180, 977-993.
42. Franck P, Garnery L, Solignac M, Cornuet JM, (1998) The origin of west European subspecies of honey bees (Apis mellifera): New insights from microsatellite and mitochondrial data. Evolution, 52, 1119-1134.
43. Garnery L, Mosshine EH, Oldroyd BP, Cornuet JM, (1995) Mitochondrial DNA variation in Moroccan and Spanish honey bee populations. Molecular Ecology, 4, 465-471.
44. Garnery L, Franck P, Baudry E, et al,. (1998a) Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica). I. Mitochondrial DNA. Genetics Selection Evolution, 30, S31-S47.
45. Garnery L, Franck P, Baudry E, et al,. (1998b) Genetic diversity of the west European honey bee (Apis mellifera mellifera and A. m. iberica). II. Microsatellite loci. Genetics Selection Evolution, 30, S49-S74.
46. Gisder S, Hedtke K, Mockel N, et al,. (2010) Five-year cohort study of Nosema spp. in Germany: Does climate shape virulence and assertiveness of Nosema ceranae? Applied and Environmental Microbiology, 76, 3032-3038.
47. Godenschwege TA, Hu HL, Shan-Crofts X, Goodman CS, Murphey RK, (2002) Bi-directional signaling by Semaphorin 1a during central synapse formation in Drosophila. Nature Neuroscience, 5, 1294-1301.
48. Gomez-Uchida D, Seeb JE, Smith MJ, et al,. (2011) Single nucleotide polymorphisms unravel hierarchical divergence and signatures of selection among Alaskan sockeye salmon (Oncorhynchus nerka) populations. BMC Evolutionary Biology, 11, 48.
49. Hardstone MC, Scott JG, (2010) Is Apis mellifera more sensitive to insecticides than other insects? Pest Management Science, 66, 1171-1180.
50. Helyar SJ, Hemmer-Hansen J, Bekkevold D, et al,. (2011) Application of SNPs for population genetics of nonmodel organisms: New opportunities and challenges. Molecular Ecology Resources, 11, 123-136.
51. Heymann Y, Steenmans C, Croissille G, Bossard M, (1994) CORINE Land Cover. Office for Official Publications of the European Communities, Luxembourg.
52. Higes M, Martin-Hernandez R, Garrido-Bailon E, et al,. (2009) Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports, 1, 110-113.
53. Higes M, Martin-Hernandez R, Meana A, (2010) Nosema ceranae in Europe: An emergent type C nosemosis. Apidologie, 41, 375-392.
54. Hollox EJ, Armour JAL, (2008) Directional and balancing selection in human beta-defensins. BMC Evolutionary Biology, 8, 113.
55. Jaffe R, Dietemann V, Allsopp MH, et al,. (2010) Estimating the density of honey bee colonies across their natural range to fill the gap in pollinator decline censuses. Conservation Biology, 24, 583-593.
56. Jiggins FM, Hurst GDD, (2003) The evolution of parasite recognition genes in the innate immune system: Purifying selection on Drosophila melanogaster peptidoglycan recognition proteins. Journal of Molecular Evolution, 57, 598-605.
57. Jin LH, Shim J, Yoon JS, et al,. (2008) Identification and functional analysis of antifungal immune response genes in Drosophila. PLoS Pathogens, 4, e1000168.
58. Johnson RM, Wen Z, Schuler MA, Berenbaum MR, (2006) Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. Journal of Economic Entomology, 99, 1046-1050.
59. Jombart T, (2008) adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
60. Joost S, Bonin A, Bruford MW, et al,. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: Towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969.
61. Joost S, Kalbermatten M, Bonin A, (2008) Spatial analysis method(SAM): A software tool combining molecular and environmental data to identify candidate loci for selection. Molecular Ecology Resources, 8, 957-960.
62. Kent CF, Issa A, Bunting AC, Zayed A, (2011) Adaptive evolution of a key gene affecting queen and worker traits in the honey bee, Apis mellifera. Molecular Ecology, 20, 5226-5235.
63. Kim TS, Maeda A, Maeda T, et al,. (2005) Delayed dark adaptation in 11-cis-retinol dehydrogenase-deficient mice- A role of RDH11 in visual processes in vivo. Journal of Biological Chemistry, 280, 8694-8704.
64. Kinel-Tahan Y, Weiss H, Dgany O, Levine A, Wides R, (2007) Drosophila odz gene is required for multiple cell types in the compound retina. Developmental Dynamics, 236, 2541-2554.
65. Kurucz E, Markus R, Zsamboki J, et al,. (2007) Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Current Biology, 17, 649-654.
66. Ladd AN, Cooper TA, (2002) Finding signals that regulate alternative splicing in the postgenomic era. Genome Biology, 3, reviews0008.
67. Lehtonen PK, Laaksonen T, Artemyev AV, et al,. (2012) Candidate genes for colour and vision exhibit signals of selection across the pied flycatcher (Ficedula hypoleuca) breeding range. Heredity, 108, 431-440.
68. Lewontin RC, Krakauer J, (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics, 74, 175-195.
69. Li X, Schuler MA, Berenbaum MR, (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annual Review of Entomology, 52, 231-253.
70. Limborg MT, Helyar SJ, de Bruyn M, et al,. (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Molecular Ecology, 21, 3686-3703.
71. Low WY, Ng HL, Morton CJ, et al,. (2007) Molecular evolution of glutathione S-transferases in the genus Drosophila. Genetics, 177, 1363-1375.
72. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P, (2003) The power and promise of population genomics: From genotyping to genome typing. Nature Reviews. Genetics, 4, 981-994.
73. Manel S, Poncet BN, Legendre P, Gugerli F, Holderegger R, (2010) Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Molecular Ecology, 19, 3824-3835.
74. Mao W, Rupasinghe SG, Johnson RM, et al,. (2009) Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 154, 427-434.
75. Mao W, Schuler MA, Berenbaum MR, (2011) CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America, 108, 12657-12662.
76. Meixner MD, Leta MA, Koeniger N, Fuchs S, (2011) The honey bees of Ethiopia represent a new subspecies of Apis mellifera-Apis mellifera simensis n. ssp. Apidologie, 42, 425-437.
77. Menzel R, Müller U, (1996) Learning and memory in honey bees: From behavior to neural substrates. Annual Review of Neuroscience, 19, 379-404.
78. Miguel I, Iriondo M, Garnery L, Sheppard WS, Estonba A, (2007) Gene flow within the M evolutionary lineage of Apis mellifera: Role of the Pyrenees, isolation by distance and post-glacial re-colonization routes in the western Europe. Apidologie, 38, 141-155.
79. Miguel I, Baylac M, Iriondo M, et al,. (2011) Both geometric morphometric and microsatellite data consistently support the differentiation of the Apis mellifera M evolutionary branch. Apidologie, 42, 150-161.
80. Moritz RFA, Kraus FB, Kryger P, Crewe RM, (2007) The size of wild honey bee populations (Apis mellifera) and its implications for the conservation of honey bees. Journal of Insect Conservation, 11, 391-397.
81. ST outlier tests for SNP loci under selection. Molecular Ecology Resources, 11, 184-194.
82. Navajas M, Migeon A, Alaux C, et al,. (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics, 9, 301.
83. Nazzi F, Brown SP, Annoscia D, et al,. (2012) Synergistic parasite-pathogen interactions mediated by host immunity can drive the collapse of honey bee colonies. PLoS Pathogens, 8, e1002735.
84. Nielsen R, (2005) Molecular signatures of natural selection. Annual Review of Genetics, 39, 197-218.
85. Nielsen D, Page RE Jr, Crosland MW, (1994) Clinal variation and selection of MDH allozymes in honey bee populations. Experientia, 50, 867-871.
86. Nielsen EE, Hemmer-Hansen J, Poulsen NA, et al,. (2009) Genomic signatures of local directional selection in a high gene flow marine organism; the Atlantic cod (Gadus morhua). BMC Evolutionary Biology, 9, 276.
87. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375-402.
88. Nunes VL, Beaumont MA, Butlin RK, Paulo OS, (2011) Multiple approaches to detect outliers in a genome scan for selection in ocellated lizards (Lacerta lepida) along an environmental gradient. Molecular Ecology, 20, 193-205.
89. Oliveira TYK, Harris EE, Meyer D, Jue CK, Silva WA, (2012) Molecular evolution of a malaria resistance gene (DARC) in primates. Immunogenetics, 64, 497-505.
90. Osborne JL, (2012) Ecology: Bumblebees and pesticides. Nature, 491, 43-45.
91. Pérez-Figueroa A, Garcia-Pereira MJ, Saura M, Rolan-Alvarez E, Caballero A, (2010) Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology, 23, 2267-2276.
92. Pilling ED, Bromleychallenor KAC, Walker CH, Jepson PC, (1995) Mechanism of synergism between the pyrethroid insecticide lambda-cyhalothrin and the imidazole fungicide prochloraz, in the honey bee (Apis mellifera L.). Pesticide Biochemistry and Physiology, 51, 1-11.
93. Pinto MA, Henriques D, Neto M, et al,. (2013) Maternal diversity patterns of Ibero-Atlantic populations reveal further complexity of Iberian honey bees. Apidologie, 44, 430-439.
94. Potts SG, Biesmeijer JC, Kremen C, et al,. (2010) Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution, 25, 345-353.
95. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
96. Prunier J, Laroche J, Beaulieu J, Bousquet J, (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Molecular Ecology, 20, 1702-1716.
97. Renaut S, Nolte AW, Rogers SM, Derome N, Bernatchez L, (2011) SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.). Molecular Ecology, 20, 545-559.
98. Riveron JM, Irving H, Ndula M, et al,. (2013) Directionally selected cytochrome P450 alleles are driving the spread of pyrethroid resistance in the major malaria vector Anopheles funestus. Proceedings of the National Academy of Sciences of the United States of America, 110, 252-257.
99. Ruttner F, (1988) Biogeography and Taxonomy of Honey Bees. Springer, Berlin.
100. Ruttner F, Tassencourt L, Louveaux J, (1978) Biometrical-statistical analysis of the geographic variability of Apis mellifera L. Apidologie, 9, 363-381.
101. Sackton TB, Lazzaro BP, Schlenke TA, et al,. (2007) Dynamic evolution of the innate immune system in Drosophila. Nature Genetics, 39, 1461-1468.
102. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
103. Schlötterer C, (2002) A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics, 160, 753-763.
104. Schluter D, Marchinko KB, Barrett RDH, Rogers SM, (2010) Natural selection and the genetics of adaptation in threespine stickleback. Philosophical Transactions of the Royal Society Series B: Biological Sciences, 365, 2479-2486.
105. Scott JG, Wen ZM, (2001) Cytochromes P450 of insects: The tip of the iceberg. Pest Management Science, 57, 958-967.
106. Sheppard WS, Meixner MD, (2003) Apis mellifera pomonella, a new honey bee subspecies from Central Asia. Apidologie, 34, 367-375.
107. Shikano T, Ramadevi J, Merilä J, (2010) Identification of local- And habitat-dependent selection: Scanning functionally important genes in nine-spined sticklebacks (Pungitius pungitius). Molecular Biology and Evolution, 27, 2775-2789.
108. Shimada Y, Shikano T, Merilä J, (2011) A high incidence of selection on physiologically important genes in the three-spined stickleback, Gasterosteus aculeatus. Molecular Biology and Evolution, 28, 181-193.
109. Smith DR, Glenn TC, (1995) Allozyme polymorphisms in spanish honey bees (Apis mellifera iberica). Journal of Heredity, 86, 12-16.
110. Smith DR, Palopoli MF, Taylor BR, et al,. (1991) Geographical overlap of two mitochondrial genomes in Spanish honey bees (Apis mellifera iberica). Journal of Heredity, 82, 96-100.
111. Somogyi K, Sipos B, Penzes Z, et al,. (2008) Evolution of genes and repeats in the Nimrod superfamily. Molecular Biology and Evolution, 25, 2337-2347.
112. Storz JF, (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology, 14, 671-688.
113. Thioulouse J, Chessel D, Doledec S, Olivier JM, (1997) ADE-4: A multivariate analysis and graphical display software. Statistics and Computing, 7, 75-83.
114. Townson SM, Chang BSW, Salcedo E, et al,. (1998) Honeybee blue-and ultraviolet-sensitive opsins: Cloning, heterologous expression in Drosophila, and physiological characterization. Journal of Neuroscience, 18, 2412-2422.
115. Tsai CJ, Sauna ZE, Kimchi-Sarfaty C, et al,. (2008) Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. Journal of Molecular Biology, 383, 281-291.
116. Tsumura Y, Uchiyama K, Moriguchi Y, Ueno S, Ihara-Ujino T, (2012) Genome scanning for detecting adaptive genes along environmental gradients in the Japanese conifer, Cryptomeria japonica. Heredity, 109, 349-360.
117. Vasemägi A, Primmer CR, (2005) Challenges for identifying functionally important genetic variation: The promise of combining complementary research strategies. Molecular Ecology, 14, 3623-3642.
118. Vitalis R, Dawson K, Boursot P, (2001) Interpretation of variation across marker loci as evidence of selection. Genetics, 158, 1811-1823.
119. 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.
120. Wang XY, Wang T, Jiao YC, von Lintig J, Montell C, (2010) Requirement for an enzymatic visual cycle in Drosophila. Current Biology, 20, 93-102.
121. Wang T, Chen GP, Zan QJ, Wang CB, Su YJ, (2012) AFLP genome scan to detect genetic structure and candidate loci under selection for local adaptation of the invasive weed Mikania micrantha. PLoS One, 7, e41310.
122. Watson FL, Puttmann-Holgado R, Thomas F, et al,. (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science, 309, 1874-1878.
123. Whitfield CW, Behura SK, Berlocher SH, et al,. (2006) Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science, 314, 642-645.
124. Wilding CS, Butlin RK, Grahame J, (2001) Differential gene exchange between parapatric morphs of Littorina saxatilis detected using AFLP markers. Journal of Evolutionary Biology, 14, 611-619.
125. Winston M, (1987) The Biology of the Honey Bee. Harvard University Press, London.
126. Wood HM, Grahame JW, Humphray S, Rogers J, Butlin RK, (2008) Sequence differentiation in regions identified by a genome scan for local adaptation. Molecular Ecology, 17, 3123-3135.
127. Yu SJ, (2002) Biochemical characteristics of microsomal and cytosolic glutathione S-transferases in larvae of the fall armyworm, Spodoptera frugiperda (J. E. Smith). Pesticide Biochemistry and Physiology, 72, 100-110.
128. Zayed A, Whitfield CW, (2008) A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera. Proceedings of the National Academy of Sciences of the United States of America, 105, 3421-3426.