Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): A model of industrial melanism

Heredity

Volumn 110, Issue 3, 2013, Pages 283-295

  Van'T Hof, A E ^a   Nguyen, P ^b   Dalikova M ^b   Edmonds, N ^a   Marec, F ^b   Saccheri, I J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

Biston betularia; Bombyx mori; melanization genes; sex chromosomes; synteny mapping

Indexed keywords

MELANIN;

CHROMOSOME; COMPARATIVE STUDY; GENOME; HYBRIDIZATION; MELANISM; MOTH; PHYLOGENETICS; SPECIATION (BIOLOGY);

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ANIMAL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIOSYNTHESIS; BOMBYX; CHROMOSOME MAP; CLASSIFICATION; EVOLUTION; GENE LOCUS; GENETIC LINKAGE; GENETICS; GENOME; INDUSTRY; INSECT CHROMOSOME; KARYOTYPING; MOTH; PHYLOGENY; SEX CHROMOSOME; SYNTENY;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; ANIMALS; BIOLOGICAL EVOLUTION; BOMBYX; CHROMOSOME MAPPING; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CHROMOSOMES, INSECT; GENETIC LINKAGE; GENETIC LOCI; GENOME, INSECT; INDUSTRY; KARYOTYPING; MELANINS; MOTHS; PHYLOGENY; SEX CHROMOSOMES; SYNTENY;

BACTERIA (MICROORGANISMS); BISTON BETULARIA; BOMBYX MORI; GEOMETRIDAE; LEPIDOPTERA; PLUTELLA XYLOSTELLA;

EID: 84873996116     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2012.84     Document Type: Article

References (92)

1. Abe H, Fujii T, Tanaka N, Yokoyama T, Kakehashi H, Ajimura M et al. (2008). Identification of the female-determining region of the W chromosome in Bombyx mori. Genetica 133: 269-282.
2. Abe H, Mita K, Yasukochi Y, Oshiki T, Shimada T (2005). Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet Genome Res 110: 144-151.
3. Abe H, Fujii T, Shimada T (2010). Sex chromosomes and sex determination in Bombyx mori. In: Goldsmith MR, Marec F (eds). Molecular Biology and Genetics of the Lepidoptera. CRC Press: Boca Raton, FL, USA. pp 65-87.
4. Andolfatto P, Scriber JM, Charlesworth B (2003). No association between mitochondrial DNA haplotypes and a female-limited mimicry phenotype in Papilio glaucus. Evolution 57: 305-316.
5. Baxter SW, Davey JW, Johnston JS, Shelton AM, Heckel DG, Jiggins CD et al. (2011). Linkage mapping and comparative genomics using next-generation RAD sequencing of a non-model organism. PLoS ONE 6: e19315.
6. Beldade P, Brakefield PM, Long AD (2002). Contribution of Distal-less to quantitative variation in butterfly eyespots. Nature 415: 315-318.
7. Beldade P, Rudd S, Gruber J, Long A (2006). A wing expressed sequence tag resource for Bicyclus anynana butterflies, an evo-devo model. BMC Genomics 7: 130.
8. Beldade P, Saenko SV, Pul N, Long AD (2009). A gene-based linkage map for Bicyclus anynana butterflies allows for a comprehensive analysis of synteny with the lepidop-teran reference genome. PLoS Genet 5: e1000366.
9. Bolshakov VN, Topalis P, Blass C, Kokoza E, Della TA, Kafatos FC et al. (2002) A comparative genomic analysis of two distant Diptera, the fruit fly, Drosophila melanogaster, and the malaria mosquito, Anopheles gambiae. Genome Res 12: 57-66.
10. Carpenter JE, Bloem S, Marec F (2005). Inherited sterility in insects. In: Dyck VA, Hendrichs J, Robinson AS (eds). Sterile Insect Technique. Principles and Practice in Area-Wide Integrated Pest Management. Springer: Dordrecht. pp 115-146.
11. Carroll S, Gates J, Keys D, Paddock S, Panganiban G, Selegue J et al. (1994). Pattern formation and eyespot determination in butterfly wings. Science 265: 109-114.
12. Conceição IC, Long AD, Gruber JD, Beldade P (2011). Genomic sequence around butterfly wing development genes: annotation and comparative analysis. PLoS ONE 6: e23778.
13. Cook LM (2003). The rise and fall of the carbonaria form of the peppered moth. Q Rev Biol 78: 399-417.
14. d'Alençon E, Sezutsu H, Legeai F, Permal E, Bernard-Samain S, Gimenez S et al. (2010). Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci USA 107: 7680-7685.
15. Daly D, Waltham K, Mulley J, Watts PC, Rosin A, Kemp SJ et al. (2004). Trinucleotide microsatellite loci for the peppered moth (Biston betularia). Mol Ecol Notes 4: 179-181.
16. Dopman EB, Bogdanowicz SM, Harrison RG (2004). Genetic mapping of sexual isolation between E and Z pheromone strains of the European corn borer (Ostrinia nubilalis). Genetics 167: 301-309.
17. Faria R, Navarro A (2010). Chromosomal speciation revisited: rearranging theory with pieces of evidence. Trends Ecol Evol 25: 660-669.
18. Ferguson L, Lee SF, Chamberlain N, Nadeau N, Joron M, Baxter S et al. (2010). Characterization of a hotspot for mimicry: assembly of a butterfly wing transcriptome to genomic sequence at the HmYb/Sb locus. Mol Ecol 19: 240-254.
19. Fujii T, Abe H, Shimada T (2010). Molecular analysis of sex chromosome-linked mutants in the silkworm Bombyx mori. J Genet 89: 365-374.
20. Fuková I, Nguyen P, Marec F (2005). Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 48: 1083-1092.
21. Futahashi R, Sato J, Meng Y, Okamoto S, Daimon T, Yamamoto K et al. (2008). yellow and ebony are the responsible genes for the larval color mutants of the silkworm Bombyx mori. Genetics 180: 1995-2005.
22. Gotter AL, Levine JD, Reppert SM (1999). Sex-linked period genes in the silkmoth, Antheraea pernyi: implications for circadian clock regulation and the evolution of sex chromosomes. Neuron 24: 953-965.
23. Gregory TR, Hebert PDN (2003). Genome size variation in lepidopteran insects. Can J Zool 81: 1399-1405.
24. Hartzer KL, Zhu KY, Baker JE (2005). Phenoloxidase in larvae of Plodia interpunctella (Lepidoptera: Pyralidae): molecular cloning of the proenzyme cDNA and enzyme activity in larvae paralyzed and parasitized by Habrobracon hebetor (Hymenoptera: Braconidae). Arch Insect Biochem Physiol 59: 67-79.
25. Heckel DG, Gahan LJ, Liu Y-B, Tabashnik BE (1999). Genetic mapping of resistance to Bacillus thuringiensis toxins in diamondback moth using biphasic linkage analysis. Proc Natl Acad Sci USA 96: 8373-8377.
26. Hirai H, Yamamoto MT, Ogura K, Satta Y, Yamada M, Taylor RW et al. (1994). Multiplication of 28S rDNA and NOR activity in chromosome evolution among ants of the Myrmecia pilosula species complex. Chromosoma 103: 171-178.
27. Imai HT, Maruyama T, Gojobori T, Inoue Y, Crozier RH (1986). Theoretical bases for karyotype evolution. 1. The minimum-interaction hypothesis. Am Nat 128: 900-920.
28. Jiggins CD, Mavarez J, Beltrán M, McMillan WO, Johnston JS, Bermingham E (2005) A genetic linkage map of the mimetic butterfly Heliconius melpomene. Genetics 171: 557-570.
29. Johnson MS, Turner JRG (1979). Absence of dosage compensation for a sex-linked enzyme in butterflies (Heliconius). Heredity 43: 71-77.
30. Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR et al. (2011). Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477: 203-206.
31. Kandul NP, Lukhtanov VA, Pierce NE (2007). Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution 61: 546-559.
32. Kapan DD, Flanagan NS, Tobler A, Papa R, Reed RD, Acevedo Gonzalez J et al. (2006). Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato. Genetics 173: 735-757.
33. Kawamura N (1988). The egg size determining gene, Esd, is a unique morphological marker on the W chromosome of Bombyx mori. Genetica 76: 195-201.
34. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL et al. (1999). Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532-534.
35. Kroemer J, Coates B, Nusawardani T, Rider S, Fraser L, Hellmich R (2011) A rearrangement of the Z chromosome topology influences the sex-linked gene display in the European corn borer, Ostrinia nubilalis. Mol Genet Genomics 286: 37-56.
36. Labandeira CC, Dilcher DL, Davis DR, Wagner DL (1994). Ninety-seven million years of angiosperm-insect association: paleobiological insights into the meaning of coevolu-tion. Proc Natl Acad Sci USA 91: 12278-12282.
37. Lees DR (1981). Industrial melanism: genetic adaptation of animals to air pollution. In: Bishop JA, Cook LM (eds). Genetic Consequences of Man Made Change. Academic Press: London. pp 129-176.
38. Linardopoulou EV, Williams EM, Fan Y, Friedman C, Young JM, Trask BJ (2005). Human subtelomeres are hot spots of interchromosomal recombination and segmental duplication. Nature 437: 94-100.
39. Lukhtanov VA (2000). Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta). J Zool Syst Evol Res 38: 73-79.
40. Majerus MEN (1998). Melanism: Evolution in Action. Oxford University Press: Oxford.
41. Marec F, Sahara K, Traut W (2010). Rise and fall of the W chromosome in Lepidoptera. In: Goldsmith MR, Marec F (eds). Molecular Biology and Genetics of the Lepidoptera. CRC Press: Boca Raton, FL, USA. pp 49-63.
42. McMillan WO, Monteiro A, Kapan DD (2002). Development and evolution on the wing. Trends Ecol Evol 17: 125-133.
43. Muller HJ (1916). The mechanism of crossing-over II. Am Nat 50: 284-305.
44. Murakami A, Imai HT (1974). Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina (Bombycidae, Lepidoptera). Chromosoma 47: 167-178.
45. Naisbit RE, Jiggins CD, Linares M, Salazar C, Mallet J (2002). Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161: 1517-1526.
46. Narita S, Nomura M, Kato Y, Fukatsu T (2006). Genetic structure of sibling butterfly species affected by Wolbachia infection sweep: evolutionary and biogeographical implications. Mol Ecol 15: 1095-1108.
47. Nokkala S (1987). Cytological characteristics of chromosome behaviour during female meiosis in Sphinx ligustri L. (Sphingidae, Lepidoptera). Hereditas 106: 169-179.
48. Pardo-Manuel de Villena F, Sapienza C (2001). Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179-1189.
49. Presgraves DC (2002). Patterns of postzygotic isolation in Lepidoptera. Evolution 56: 1168-1183.
50. Pringle EG, Baxter SW, Webster CL, Papanicolaou A, Lee SF, Jiggins CD (2007). Synteny and chromosome evolution in the Lepidoptera: evidence from mapping in Heliconius melpomene. Genetics 177: 417-426.
51. Prowell DP (1998). Sex linkage and speciation in Lepidoptera. In: Howard DJ, Berlocher SH (eds). Endless Forms: Species and Speciation. Oxford University Press: Oxford. pp 309-319.
52. Putnam AS, Scriber JM, Andolfatto P (2007). Discordant divergence times among Z-chromosome regions between two ecologically distinct swallowtail butterfly species. Evolution 61: 912-927.
53. Reed RD, Nagy LM (2005). Evolutionary redeployment of a biosynthetic module: expression of eye pigment genes vermilion, cinnabar, and white in butterfly wing development. Evol Dev 7: 301-311.
54. Reed RD, Serfas MS (2004). Butterfly wing pattern evolution is associated with changes in a Notch/Distal-less temporal pattern formation process. Curr Biol 14: 1159-1166.
55. Regier JC (2007). Protocols, concepts, and reagents for preparing DNA sequencing templates. wwwumbiumdedu/users/jcrlab/PCR-primerspdf.
56. Sahara K, Marec F, Traut W (1999). TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7: 449-460.
57. Sahara K, Yoshido A, Kawamura N, Ohnuma A, Abe H, Mita K et al. (2003). W-derived BAC probes as a new tool for identification of the W chromosome and its aberrations in Bombyx mori. Chromosoma 112: 48-55.
58. Sahara K, Yoshido A, Marec F, Fuková I, Zhang H-B, Wu C-C et al. (2007). Conserved synteny of genes between chromosome 15 of Bombyx mori and a chromosome of Manduca sexta shown by five-color BAC-FISH. Genome 50: 1061-1065.
59. Schlecht HB, Lichten M, Goldman ASH (2004). Compartmentalization of the yeast meiotic nucleus revealed by analysis of ectopic recombination. Genetics 168: 1189-1203.
60. Shibata F, Sahara K, Naito Y, Yasukochi Y (2009). Reprobing multicolor FISH preparations in lepidopteran chromosome. Zool Sci 26: 187-190.
61. Singh ND, Larracuente AM, Sackton TB, Clark AG (2009). Comparative genomics on the Drosophila phylogenetic tree. Annu Rev Ecol Evol Syst 40: 459-480.
62. Sturtevant AH (1913). The linear arrangement of six sex-linked factors in Drosophila, as shown by their mode of association. J Exp Zool 14: 43-59.
63. Suomalainen E (1969). Chromosome evolution in the Lepidoptera. Chromosomes Today 2: 132-138.
64. Suomalainen E, Brown KSJ (1984). Chromosome number variation within Philaethria butterflies (Lepidoptera: Nymphalidae, Heliconiini). Chromosoma 90: 170-176.
65. Suzuki MG (2010). Sex determination: insights from the silkworm. J Genet 89: 357-363.
66. Suzuki MG, Shimada T, Kobayashi M (1999). Bm kettin, homologue of the Drosophila kettin gene, is located on the Z chromosome in Bombyx mori and is not dosage compensated. Heredity 82: 170-179.
67. Talbert PB, Bayes JJ, Henikoff S (2009). Evolution of centromeres and kinetochores: A two-part fugue. In: De Wulf P, Earnshaw WC (eds). The Kinetochore: From Molecular Discoveries to Cancer Therapy. Springer: New York. pp 193-229.
68. The Heliconius Genome Consortium (2012). Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94-98.
69. The International Silkworm Genome Consortium (2008). The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38: 1036-1045.
70. Traut W (1977). A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of Ephestia kuehniella (Lepidoptera). Genetica 47: 135-142.
71. Traut W, Marec F (1996). Sex chromatin in Lepidoptera. Q Rev Biol 71: 239-256.
72. Traut W, Sahara K, Marec F (2007). Sex chromosomes and sex determination in Lepidoptera. Sex Dev 1: 332-346.
73. Traut W, Scholz D (1978). Structure, replication and transcriptional activity of the sex-specific heterochromatin in a moth. Exp Cell Res 113: 85-94.
74. Van Nieukerken EJ, Kaila L, Kitching IJ, Kristensen NP, Lees DC, Minet J et al. (2011). Order Lepidoptera Linnaeus, 1758. Zootaxa 3148: 212-221.
75. Van't Hof AE, Edmonds E, Dalíková M, Marec F, Saccheri IJ (2011). Industrial melanism in British peppered moths has a singular and recent mutational origin. Science 332: 958-960.
76. Van't Hof AE, Marec F, Saccheri IJ, Brakefield PM, Zwaan BJ (2008). Cytogenetic characterization and AFLP-based genetic linkage mapping for the Butterfly Bicyclus anynana, covering all 28 karyotyped chromosomes. PLoS ONE 3: e3882.
77. Van't Hof AE, Saccheri IJ (2010). Industrial melanism in the peppered moth is not associated with genetic variation in canonical melanisation gene candidates. PLoS ONE 5: e10889.
78. Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M et al. (1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23: 4407-4414.
79. Wang B, Porter AH (2004). An AFLP-based interspecific linkage map of sympatric, hybridizing Colias butterflies. Genetics 168: 215-225.
80. Wang J, Xia Q, He X, Dai M, Ruan J, Chen J et al. (2005). SilkDB: a knowledgebase for silkworm biology and genomics. Nucleic Acids Res 33: D399-D402.
81. Weatherbee SD, Nijhout HF, Grunert LW, Halder G, Galant R, Selgue J et al. (1999). Ultrabithorax function in butterfly wings and the evolution of insect wing patterns Curr Biol 9: 109-115.
82. White MJD (1973). Animal Cytology and Evolution. Cambridge University Press: Cambridge.
83. Winter CB, Porter AH (2010). AFLP linkage map of hybridizing swallowtail butterflies, Papilio glaucus and Papilio canadensis. J Hered 101: 83-90.
84. Wrensch DL, Kethley JB, Norton RA (1994). Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. In: Houck M (ed.). Mites: Ecological and Evolutionary Analyses of Life-History Patterns. Chapman & Hall: New York. pp 282-342.
85. Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B et al. (2004). A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306: 1937-1940.
86. Yamamoto K, Nohata J, Kadono-Okuda K, Narukawa J, Sasanuma M, Sasanuma S et al. (2008). A BAC-based integrated linkage map of the silkworm, Bombyx mori Genome Biol 9: R21.
87. Yasukochi Y (1998). A dense genetic map of the silkworm, Bombyx mori, covering all chromosomes based on 1018 molecular markers. Genetics 150: 1513-1525.
88. Yasukochi Y, Ashakumary LA, Baba K, Yoshido A, Sahara K (2006). A second-generation integrated map of the silkworm reveals synteny and conserved gene order between lepidopteran insects. Genetics 173: 1319-1328.
89. Yasukochi Y, Tanaka-Okuyama M, Shibata F, Yoshido A, Marec F, Wu C et al. (2009). Extensive conserved synteny of genes between the karyotypes of Manduca sexta and Bombyx mori revealed by BAC-FISH mapping. PLoS ONE 4: e7465.
90. Yoshido A, Sahara K, Marec F, Matsuda Y (2011). Step-by-step evolution of neo-sex chromosomes in geographical populations of wild silkmoths, Samia cynthia ssp. Heredity 106: 614-624.
91. Zedek F, Bureš P (2012). Evidence for centromere drive in the holocentric chromosomes of Caenorhabditis. PLoS ONE 7: e30496.
92. Zhan S, Merlin C, Boore JL, Reppert SM (2011). The monarch butterfly genome yields insights into long-distance migration. Cell 147: 1171-1185.