Positive selection has driven the evolution of the drosophila Insulin-Like Receptor (InR) at different timescales

Molecular Biology and Evolution

Volumn 26, Issue 8, 2009, Pages 1723-1732

  Guirao Rico, Sara ^a   Aguadé, Montserrat ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Drosophila; Insulin receptor; Nucleotide polymorphism; Positive selection

Indexed keywords

DNA; INSULIN RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; DNA SEQUENCE; DROSOPHILA; DROSOPHILA MELANOGASTER; GENE SEQUENCE; GENETIC POLYMORPHISM; INR GENE; MOLECULAR EVOLUTION; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PREDICTION; RECEPTOR GENE; SPECIES COMPARISON;

ANIMALS; DROSOPHILA; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; PHYLOGENY; RECEPTOR PROTEIN-TYROSINE KINASES; SELECTION (GENETICS);

DROSOPHILA MELANOGASTER; SOPHOPHORA;

EID: 67749139731     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msp088     Document Type: Article

References (81)

1. Andersen AS, Kjeldsen T, Wiberg FC, Vissing H, Schaffer L, Rasmussen JS, De Meyts P, Moller NP. 1992. Identification of determinants that confer ligand specificity on the insulin receptor. J Biol Chem. 267:13681-13686.
2. Andolfatto P. 2001. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 18:279-290.
3. Andolfatto P. 2005. Adaptive evolution of non-coding DNA in Drosophila. Nature. 437:1149-1152.
4. Ashburner M. 1989. Drosophila: a laboratory handbook. New York: Cold Spring Harbor Laboratory Press.
5. Begun DJ, Holloway AK, Stevens K, et al. (13 co-authors). 2007. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5:e310.
6. Begun DJ, Whitley P. 2000. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci USA. 97:5960-5965.
7. Benyoucef S, Surinya KH, Hadaschik D, Siddle K. 2007. Characterization of insulin/IGF hybrid receptors: contributions of the insulin receptor L2 and Fn1 domains and the alternatively spliced exon 11 sequence to ligand binding and receptor activation. Biochem J. 403:603-613.
8. Bergman CM, Kreitman M. 2001. Analysis of conserved non-coding DNA in Drosophila reveals similar constraints in intergenic and intronic sequences. Genome Res. 11:1335-1345.
9. Betancourt AJ, Presgraves DC. 2002. Linkage limits the power of natural selection in Drosophila. Proc Natl Acad Sci USA. 99:13616-13620.
10. Bishop NA, Guarente L. 2007. Genetic links between diet and lifespan: shared mechanisms from yeast to humans. Nat Rev Genet. 8:835-844.
11. Broughton SJ, Piper MD, Ikeya T, et al. (11 co-authors). 2005. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA. 102:3105-3110.
12. Calboli FC, Kennington WJ, Partridge L. 2003. QTL mapping reveals a striking coincidence in the positions of genomic regions associated with adaptive variation in body size in parallel clines of Drosophila melanogaster on different continents. Evolution. 57:2653-2658.
13. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552.
14. Clancy DJ, Gems D, Harshman LG, Oldham S, Stocker H, Hafen E, Leevers SJ, Partridge L. 2001. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science. 292:104-106.
15. Clark AG, Eisen MB, Smith DR, et al. (417 co-authors). 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature. 450:203-218.
16. David JR, Capy P. 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4:106-111.
17. De Meyts P. 2004. Insulin and its receptor: structure, function and evolution. Bioessays. 26:1351-1362.
18. De Meyts P, Whittaker J. 2002. Structural biology of insulin and IGF1 receptors: implications for drug design. Nat Rev Drug Discov. 1:769-783.
19. Eyre-Walker A. 2002. Changing effective population size and the McDonald-Kreitman test. Genetics. 162:2017-2024.
20. Fay JC, Wu CI. 2000. Hitchhiking under positive Darwinian selection. Genetics. 155:1405-1413.
21. Fernandez-Almonacid R, Rosen OM. 1987. Structure and ligand specificity of the Drosophila melanogaster insulin receptor. Mol Cell Biol. 7:2718-2727.
22. Fernandez R, Tabarini D, Aspiazu N, Frasch M, Schlessinger J. 1995. The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potencial. EMBO J. 14:3373-3384.
23. Fu YX, Li WH. 1993. Statistical tests of neutrality of mutations. Genetics. 133:693-709.
24. Garofalo RS. 2002. Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol Metab. 13:156-162.
25. Garza-Garcia A, Patel DS, Gems D, Driscoll PC. 2007. RILM: a web-based resource to aid comparative and functional analysis of the insulin and IGF-1 receptor family. Hum Mutat. 28:660-668.
26. Giannakou ME, Partridge L. 2007. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem Sci. 32:180-188.
27. Goberdhan DC, Wilson C. 2003. The functions of insulin signaling: size isn't everything, even in Drosophila. Differentiation. 71:375-397.
28. Gockel J, Robinson SJ, Kennington WJ, Goldstein DB, Partridge L. 2002. Quantitative genetic analysis of natural variation in body size in Drosophila melanogaster. Heredity. 89:145-153.
29. Goldman N, Yang Z. 1994. A codon-based model of nucleotide substitution for protein-coding DNA sequences. Mol Biol Evol. 11:725-736.
30. Guex N, Peitsch MC. 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 18:2714-2723.
31. Halligan DL, Eyre-Walker A, Andolfatto P, Keightley PD. 2004. Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Res. 14:273-279.
32. HudsonRR.1990.Genegenealogiesandthe coalescent process.In: Antonovics J, Futuyma D, editors. Oxford surveys in evolutionary biology. Oxford: Oxford University Press. p. 1-44.
33. Ikeya T, Galic M, Belawat P, Nariz K, Hafen E. 2002. Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol. 12:1293-1300.
34. Johnston LA, Gallant P. 2002. Control of growth and organ size in Drosophila. Bioessays. 24:54-64.
35. Jukes TH, Cantor CR. 1969. Evolution of protein molecules. In: Munro HN, editor. Mammalian protein metabolism. New York: Academic Press. p. 21-123.
36. Kennington WJ, Partridge L, Hoffmann AA. 2006. Patterns of diversity and linkage disequilibrium within the cosmopolitan inversion In(3R)Payne in Drosophila melanogaster are indicative of coadaptation. Genetics. 172:1655-1663.
37. Kjeldsen T, Andersen AS, Wiberg FC, Rasmussen JS, Schaffer L, Balschmidt P, Moller KB, Moller NP. 1991. The ligand specificities of the insulin receptor and the insulinlike growth factor I receptor reside in different regions of a common binding site. Proc Natl Acad Sci USA. 88:4404-4408.
38. Lachaise D, Cariou LM, David JR, Lemeunier F, Tsacas L, Ashburner M. 1988. Historical biogeography of the Drosophila melanogaster species subgroup. Evol Biol. 22: 159-225.
39. LeRoith D. 1995. A novel Drosophila insulin receptor: fly in the ointment or evolutionary conservation? Endocrinology. 136:2355-2356.
40. Maddison WP, Maddison DR. 1992. MacClade: analysis of phylogeny and character evolution. Version 3. Sunderland (MA): Sinauer Associates.
41. McClellan DA, Palfreyman EJ, Smith MJ, Moss JL, Christensen RG, Sailsbery JK. 2005. Physicochemical evolution and molecular adaptation of the cetacean and artiodactyl cytochrome b proteins. Mol Biol Evol. 22:437-455.
42. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 351:652-654.
43. McKern NM, Lawrence MC, Streltsov VA, et al. (23 co-authors). 2006. Structure of the insulin receptor ectodomain reveals a folded-over conformation. Nature. 443:218-221.
44. Moriyama EN, Powell JR. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 13:261-277.
45. Nei M. 1987. Molecular evolutionary genetics. New York: Columbia University Press.
46. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426.
47. Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 148:929-936.
48. Oldham S, Hafen E. 2003. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13:79-85.
49. Pitnick S, Markow TA, Spicer GS. 1995. Delayed male maturity is a cost of producing large sperm in Drosophila. Proc Natl Acad Sci USA. 92:10614-10618.
50. Pollard DA, Iyer VN, Moses AM, Eisen MB. 2006. Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting. PLoS Genet. 2:e173.
51. Posada D, Crandall KA. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics. 14:817-818.
52. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19:2496-2497.
53. Ruan Y, Chen C, Cao Y, Garofalo RS. 1995. The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction. J Biol Chem. 270:4236-4243.
54. Rychlik W. 1992. OLIGO 4.06 primer analysis software. lymouth (MN): National Biosciences Inc.
55. Saltiel AR, Kahn CR. 2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 414:799-806.
56. Saucedo LJ, Edgar BA. 2002. Why size matters: altering cell size. Curr Opin Genet Dev. 12:565-571.
57. Sokal RR, Rohlf FJ. 1995. Biometry. New York: W.H. Freeman.
58. Stocker H, Hafen E. 2000. Genetic control of cell size. Curr Opin Genet Dev. 10:529-535.
59. Sturtevant AH. 1939. On the subdivision of the genus Drosophila. Proc Natl Acad Sci USA. 25:137-141.
60. Suzuki Y, Nei M. 2004. False-positive selection identified by ML-based methods: examples from the Sig1 gene of the diatom Thalassiosira weissflogii and the tax gene of a human T-cell lymphotropic virus. Mol Biol Evol. 21:914-921.
61. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
62. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochon-drial DNA in humans and chimpanzees. Mol Biol Evol. 10: 512-526.
63. Tamura K, Subramanian S, Kumar S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol. 21:36-44.
64. Tatar M. 2004. The neuroendocrine regulation of Drosophila aging. Exp Gerontol. 39:1745-1750.
65. Thompson JD, Higgins DG, Gibson TJ. 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.
66. Ward C, Lawrence M, Streltsov V, Garrett T, McKern N, Lou MZ, Lovrecz G, Adams T. 2008. Structural insights into ligand-induced activation of the insulin receptor. Acta Physiol (Oxf). 192:3-9.
67. Whelan S, Goldman N. 1999. Distributions of statistics used for the comparison of models of sequence evolution in phylogenetics. Mol Biol Evol. 16:1292-1299.
68. Woolley S, Johnson J, Smith MJ, Crandall KA, McClellan DA. 2003. TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics. 19:671-672.
69. Wu Q, Brown MR. 2006. Signaling and function of insulin-like peptides in insects. Annu Rev Entomol. 51:1-24.
70. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
71. Yang Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol. 15:568-573.
72. Yang Z, Nielsen R. 1998. Synonymous and nonsynonymous rate variation in nuclear genesofmammals. J Mol Evol. 46:409-418.
73. Yang Z, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 19:908-917.
74. Yang Z, Nielsen R, Goldman N, Pedersen AM. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics. 155:431-449.
75. Yang Z, Swanson WJ. 2002. Codon-substitution models to detect adaptive evolution that account for heterogeneous selective pressures among site classes. Mol Biol Evol. 19: 49-57.
76. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
77. Yenush L, Fernandez R, Myers MG Jr., Grammer TC, Sun XJ, Blenis J, Pierce JH, Schlessinger J, White MF. 1996. The Drosophila insulin receptor activates multiple signaling pathways but requires insulin receptor substrate proteins for DNA synthesis. Mol Cell Biol. 16:2509-2517.
78. Zhang J. 2004. Frequent false detection of positive selection by the likelihood method with branch-site models. Mol Biol Evol. 21:1332-1339.
79. Zhang J, Nielsen R, Yang Z. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 22:2472-2479.
80. Zhang Y. 2007. Template-based modeling and free modeling by I-TASSER in CASP7. Proteins. 69:108-117.
81. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 9(Suppl 8):40.