Deficiency screening for genomic regions with effects on environmental sensitivity of the sensory bristles of drosophila melanogaster

Evolution

Volumn 66, Issue 9, 2012, Pages 2878-2890

  Takahashi, Kazuo H ^a   Okada, Yasukazu ^a   Teramura, Kouhei ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Developmental stability; Environmental sensitivity; Fluctuating asymmetry; Isogenic deficiency strains; Reaction norm

Indexed keywords

CORRELATION; EVOLUTIONARY BIOLOGY; FLY; GENOMICS; MUTATION; PHENOTYPE; PHENOTYPIC PLASTICITY; SENSORY SYSTEM;

DROSOPHILA MELANOGASTER;

EID: 85027924055     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01636.x     Document Type: Article

References (65)

1. Adams, M. D., S. E. Celniker, R. A. Holt, C. A. Evans, J. D. Gocayne, P. G. Amanatides, S. E. Scherer, P. W. Li, R. A. Hoskins, R. F. Galle, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
2. Benjamini, Y., and Y. Hochberg 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B. 57:289-300.
3. Breuker, C. J., J. S. Patterson, and C. P. Klingenberg 2006. A single basis for developmental buffering of Drosophila wing shape. PLoS One 1:e7.
4. Bronmark, C., and J. G. Miner 1992. Predator-induced phenotypical change in body morphology in crucian carp. Science 258:1348-1350.
5. Bubliy, O. A., A. G. Imasheva, and V. Loeschcke 2000. Half-sib analysis of three morphological traits in Drosophila melanogaster under poor nutrition. Hereditas 133:59-63.
6. Cohen, J. 1973. Eta-squared and partial eta-squared in fixed factor ANOVA designs. Educ. Psychol. Meas. 33:107-112.
7. Crews, D., J. M. Bergeron, J. J. Bull, D. Flores, A. Tousignant, J. K. Skipper, and T. Wibbels 1994. Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications. Dev. Genet. 15:297-312.
8. Debat, V., and P. David 2001. Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol. Evol. 16:555-561.
9. Debat, V., C. C. Milton, S. Rutherford, C. P. Klingenberg, and A. A. Hoffmann 2006. HSP90 and the quantitative variation of wing shape in Drosophila melanogaster. Evolution 60:2529-2538.
10. Debat, V., A. Debelle, and I. Dworkin 2009. Plasticity, canalization, and developmental stability of the Drosophila wing: joint effects of mutations and developmental temperature. Evolution 63:2864-2876.
11. Dilda, C. L., and T. F. Mackay 2002. The genetic architecture of Drosophila sensory bristle number. Genetics 162:1655-1674.
12. Dubnau, J., A. S. Chiang, L. Grady, J. Barditch, S. Gossweiler, J. McNeil, P. Smith, F. Buldoc, R. Scott, U. Certa, et al. 2003. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13:286-296.
13. Dworkin, I. 2005a. Evidence for canalization of distal-less function in the leg of Drosophila melanogaster. Evol. Dev. 7:89-100.
14. Dworkin, I. 2005b. A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster. Evolution 59:1500-1509.
15. Flatt, T. 2005. The evolutionary genetics of canalization. Q. Rev. Biol. 80:287-316.
16. Gause, G. F. 1947. Problems of evolution. Trans. Connect. Acad. Arts Sci. 37:17-68.
17. Gerber, A. P., S. Luschnig, M. A. Krasnow, P. O. Brown, and D. Herschlag 2006. Genomewide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 103:4487-4492.
18. Gurganus, M. C., J. D. Fry, S. V. Nuzhdin, E. G. Pasyukova, R. F. Lyman, and T. F. Mackay 1998. Genotype-environment interaction at quantitative trait loci affecting sensory bristle number in Drosophila melanogaster. Genetics 149:1883-1898.
19. Gurganus, M. C., S. V. Nuzhdin, J. W. Leips, and T. F. Mackay 1999. High-resolution mapping of quantitative trait loci for sternopleural bristle number in Drosophila melanogaster. Genetics 152:1585-1604.
20. Gutteling, E. W., J. A. Riksen, J. Bakker, and J. E. Kammenga 2007. Mapping phenotypic plasticity and genotype-environment interactions affecting life-history traits in Caenorhabditis elegans. Heredity 98:28-37.
21. Haag-Liautard, C., M. Dorris, X. Maside, S. Macaskill, D. L. Halligan, D. Houle, B. Charlesworth, and P. D. Keightley 2007. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445:82-85.
22. Hallgrimsson, B., and B. K. Hall, eds. 2005. Variation. Elsevier Academic Press, Burlington
23. Hollander, J. 2008. Testing the grain-size model for the evolution of phenotypic plasticity. Evolution 62:1381-1389.
24. Huerta-Sanchez, E., and R. Durrett 2007. Wagner's canalization model. Theor. Popul. Biol. 71:121-130.
25. Kellermann, V. M., A. A. Hoffmann, and C. M. Sgro 2007. Hsp90 inhibition and the expression of phenotypic variability in the rainforest species Drosophila birchii. Biol. J. Linn. Soc. 92:457-465.
26. Klingenberg, C. P., and G. S. McIntyre 1998. Geometric morphometrics of developmental instability: analyzing patterns of fluctuating asymmetry with procrustes methods. Evolution 52:1363-1375.
27. Lacaze, X., P. M. Hayes, and A. Korol 2009. Genetics of phenotypic plasticity: QTL analysis in barley, Hordeum vulgare. Heredity 102:163-173.
28. Leamy, L. J., E. J. Routman, and J. M. Cheverud 1998. Quantitative trait loci for fluctuating asymmetry of discrete skeletal characters in mice. Heredity 80:509-518.
29. Leung, B., M. R. Forbes, and D. Houle 2000. Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am. Nat. 155:101-115.
30. Levine, T. R., and C. R. Hullett 2006. Eta squared, partial eta squared, and misreporting of effect size in communication research. Hum. Commun. Res. 28:612-625.
31. Liefting, M., A. A. Hoffmann, and J. Ellers 2009. Plasticity versus environmental canalization: population differences in thermal responses along a latitudinal gradient in Drosophila serrata. Evolution 63:1954-1963.
32. Mackay, T. F. 1996. The nature of quantitative genetic variation revisited: lessons from Drosophila bristles. Bioessays 18:113-121.
33. Meiklejohn, C. D., and D. L. Hartl 2002. A single mode of canalization. Trends Ecol. Evol. 17:468-473.
34. Milton, C. C., B. Huynh, P. Batterham, S. Rutherford, and A. A. Hoffmann 2003. Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability. Proc. Natl. Acad. Sci. USA 100:13396-13401.
35. Milton, C. C., P. Batterham, J. A. McKenzie, and A. A. Hoffmann 2005. Effect of E (sev) and Su (Raf) Hsp83 mutants and trans-heterozygotes on bristle trait means and variation in Drosophila melanogaster. Genetics 171:119-130.
36. Moller, A. P., and J. P. Swaddle 1997. Asymmetry, developmental stability, and evolution. Oxford Univ. Press, Oxford, U.K.
37. Norga, K. K., M. C. Gurganus, C. L. Dilda, A. Yamamoto, R. F. Lyman, P. H. Patel, G. M. Rubin, R. A. Hoskins, T. F. Mackay, and H. J. Bellen 2003. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr. Biol. 13:1388-1396.
38. Nuzhdin, S. V., P. D. Keightley, E. G. Pasyukova, and E. A. Morozova 1998. Mapping quantitative trait loci affecting sternopleural bristle number in Drosophila melanogaster using changes of marker allele frequencies in divergently selected lines. Genet. Res. 72:79-91.
39. Palmer, A. R., and K. Strobeck 2003. Fluctuating asymmetry analysis revisited. Pp. 279-319 in M. Polak, ed. Developmental instability: causes and consequences. Oxford Univ. Press, Oxford, U.K
40. Palmer, R. A., and C. Strobeck 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu. Rev. Ecol. Syst. 17:391-421.
41. Parisi, M., and H. Lin 1999. The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis. Genetics 153:235-250.
42. Pelabon, C., M. L. Carlson, T. M. Hansen, N. G. Yoccoz, and W. S. Armbruster 2004. Consequences of inter-population crosses on developmental stability and canalization of floral traits in Dalechampia scandens (Euphorbiaceae). J. Evol. Biol. 17:19-32.
43. Pigllucci, M. 1996. How organisms respond to environmental changes: from phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11:168-173.
44. Queitsch, C., T. A. Sangster, and S. Lindquist 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.
45. Rego, C., M. Matos, and M. Santos 2006. Symmetry breaking in interspecific drosophila hybrids is not due to developmental noise. Evoluion 60:746-761.
46. Roskam, J. C., and P. M. Brakefield 1996. A comparison of temperature-induced polyphenism in African Bicyclus butterflies from a seasonal savannah-rainforest ecotone. Evolution 50:2360-2372.
47. Roskam, J. C., and P. M. Brakefield 1999. Seasonal polyphenism in Bicyclus (Lepidoptera: Satyridae) butterflies: different climates need different cues. Biol. J. Linn. Soc. 66:345-356.
48. Rutherford, S., and S. Lindquist 1998. Hsp90 as a capacitor for morphological evolution. Nature 396:336-342.
49. Ryder, E., B. Fiona, A. Michael, B.-L. Rosa, C. Darin, D. Jenny, W. Jane, G. David, G. Nicola, J. Glynnis, et al. 2004. The DrosDel collection: a set of P-element insertions for generating custom chromosomal aberrations in Drosophila melanogaster. Genetics 167:797-813.
50. Ryder, E., M. Ashburner, R. Bautista-Llacer, J. Drummond, J. Webster, G. Johnson, T. Morley, Y. S. Chan, F. Blows, D. Coulson, et al. 2007. The DrosDel deletion collection: a Drosophila genomewide chromosomal deficiency resource. Genetics 177:615-629.
51. Santos, M., P. F. Iriarte, and W. Cespedes 2005. Genetics and geometry of canalization and developmental stability in Drosophila subobscura. BMC Evol. Biol. 5:7.
52. Schweers, B. A., K. J. Walters, and M. Stern 2002. The Drosophila melanogaster translational repressor pumilio regulates neuronal excitability. Genetics 161:1177-1185.
53. Sgro, C. M., B. Wegener, and A. A. Hoffmann 2010. A naturally occurring variant of Hsp90 that is associated with decanalization. Proc. Biol. Sci. 277:2049-2057.
54. Stearns, S. C., and T. J. Kawecki 1994. Fitness sensitivity and the canalization of life-history traits. Evolution 48:1438-1450.
55. Stearns, S. C., M. Kaiser, and T. J. Kawecki 1995. The differential genetic and environmental canalization of fitness components in Drosophila melanogaster. J. Evol. Biol. 8:539-557.
56. Szakmary, A., D. N. Cox, Z. Wang, and H. Lin 2005. Regulatory relationship among piwi, pumilio, and bag-of-marbles in Drosophila germline stem cell self-renewal and differentiation. Curr. Biol. 15:171-178.
57. Takahashi, K. H., L. Rako, T. Takano-Shimizu, A. A. Hoffmann, and S. F. Lee 2010. Effects of small Hsp genes on developmental stability and microenvironmental canalization. BMC Evol. Biol. 10:284.
58. Takahashi, K. H., P. J. Daborn, A. A. Hoffmann, and T. Takano-Shimizu 2011a. Environmental stress-dependent effects of deletions encompassing Hsp70Ba on canalization and quantitative trait asymmetry in Drosophila melanogaster. PLoS One 6:e17295.
59. Takahashi, K. H., Y. Okada, and K. Teramura 2011b. Genome-wide deficiency mapping of the regions responsible for temporal canalization of the developmental processes of Drosophila melanogaster. J. Hered. 102:448-457.
60. Takahashi, K. H., Y. Okada, and K. Teramura 2011c. Genome-wide deficiency screen for the genomic regions responsible for heat resistance in Drosophila melanogaster. BMC Genet. 12:57.
61. Takahashi, K. H., Y. Okada, K. Teramura, and M. Tsujino 2011d. Deficiency mapping of the genomic regions associated with effects on developmental stability in Drosophila melanogaster. Evolution 65:3565-3577.
62. Waddington, C. H. 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563-565.
63. Wagner, G. P., G. Booth, and H. Bagheri-Chaichian 1997. A population genetic theory of canalization. Evolution 51:329-347.
64. Woltereck, R. 1909. Weitere experimentelle Untersuchungen über Artveränderung, speziel über das Wesen quantitativer Artunterschiede bei Daphnien. Verh. Dtsch. Zool. Ges. 19:110-173.
65. Yeyati, P. L., R. M. Bancewicz, J. Maule, and V. van Heyningen 2007. Hsp90 selectively modulates phenotype in vertebrate development. PLoS Genet. 3:e43.