A highly pleiotropic amino acid polymorphism in the Drosophila insulin receptor contributes to life-history adaptation

Evolution

Volumn 68, Issue 12, 2014, Pages 3395-3409

  Paaby, Annalise B ^a,b   Bergland, Alan O ^c   Behrman, Emily L ^a   Schmidt, Paul S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Adaptation; Cline; InR; Pleiotropy; Seasonality

Indexed keywords

AMINO ACID; DROSOPHILA PROTEIN; INR PROTEIN, DROSOPHILA; PROTEIN TYROSINE KINASE;

ADAPTATION; ANIMAL; BODY SIZE; DROSOPHILA; FERTILITY; GENE FREQUENCY; GENE LOCUS; GENETIC POLYMORPHISM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLEIOTROPY; SEASON; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; AMINO ACIDS; ANIMALS; BASE SEQUENCE; BODY SIZE; DROSOPHILA; DROSOPHILA PROTEINS; FERTILITY; GENE FREQUENCY; GENETIC LOCI; GENETIC PLEIOTROPY; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; RECEPTOR PROTEIN-TYROSINE KINASES; SEASONS; SIGNAL TRANSDUCTION;

EID: 84914133448     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12546     Document Type: Article

References (75)

1. Anderson, A. R., J. E. Collinge, A. A. Hoffmann, M. Kellett, and S. W. McKechnie . 2003. Thermal tolerance trade-offs associated with the right arm of chromosome 3 and marked by the hsr-omega gene in Drosophila melanogaster. Heredity 90:195-202.
2. Anderson, J. L., R. M. Reynolds, L. T. Morran, J. Tolman-Thompson, and P. C. Phillips . 2011a. Experimental evolution reveals antagonistic pleiotropy in reproductive timing but not life span in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 66:1300-1308.
3. Anderson, J. T., J. H. Willis, and T. Mitchell-Olds . 2011b. Evolutionary genetics of plant adaptation. Trends Genet. 27:258-266.
4. Bansal, V. 2010. A statistical method for the detection of variants from next-generation resequencing of DNA pools. Bioinformatics 26:i318-i324.
5. Benjamini, B., and Y. Hochberg . 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B 57:289-300.
6. Bergland, A. O., H. S. Chae, Y. J. Kim, and M. Tatar . 2012. Fine-scale mapping of natural variation in fly fecundity identifies neuronal domain of expression and function of an aquaporin. PLOS Genet. 8:e1002631.
7. Bergland, A. O., E. L. Behrman, K. R. O'Brien, P. S. Schmidt, and D. A. Petrov . 2014. Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila. PLOS Genet. 10:e1004775.
8. Bock, I. R., and P. A. Parsons . 1981. Species of Australia and New Zealand. Pp. 291-308 in M. Ashburner, H. L. Carson, J. N. Thompson, eds. Genetics and biology of Drosophila. Academic Press, Lond.
9. Capy, P., E. Pla, and J. R. David . 1993. Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and Drosophila simulans. Evolution 25:517-536.
10. Carbone, M. A., K. W. Jordan, R. F. Lyman, S. T. Harbison, J. Leips, T. J. Morgan, M. DeLuca, P. Awadalla, and T. F. Mackay . 2006. Phenotypic variation and natural selection at catsup, a pleiotropic quantitative trait gene in Drosophila. Curr. Biol. 16:912-919.
11. Casas-Tinto, S., M. T. Marr, P. Andreu, and O. Puig . 2007. Characterization of the Drosophila insulin receptor promoter. Biochim. Biophys. Acta 1769:236-243.
12. Clancy, D. J., D. Gems, L. G. Harshman, S. Oldham, H. Stocker, E. Hafen, S. J. Leevers, and L. Partridge . 2001. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292:104-106.
13. Dantzer, B., and E. M. Swanson . 2012. Mediation of vertebrate life histories via insulin-like growth factor-1. Biol. Rev. Camb. Philos. Soc. 87:414-429.
14. David, J. R., and C. Bocquet . 1975. Evolution in a cosmopolitan species: genetic latitudinal clines in Drosophila melanogaster wild populations. Experientia 31:164-166.
15. David, J. R., and P. Capy . 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4:106-111.
16. De Jong, G., and Z. Bochdanovits . 2003. Latitudinal clines in Drosophila melanogaster: body size, allozyme frequencies, inversion frequencies, and the insulin-signalling pathway. J. Genet. 82:207-223.
17. De Luca, M., N. V. Roshina, G. L. Geiger-Thornsberry, R. F. Lyman, E. G. Pasyukova, and T. F. Mackay . 2003. Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat. Genet. 34:429-433.
18. Fabian, D. K., M. Kapun, V. Nolte, R. Kofler, P. S. Schmidt, C. Schlotterer, and T. Flatt . 2012. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America. Mol. Ecol. 21:4748-4769.
19. Flatt, T., and A. Heyland . 2011. Mechanisms of life history evolution: the genetics and physiology of life history traits and trade-offs. Oxford Univ. Press, New York.
20. Flatt, T., K. J. Min, C. D'Alterio, E. Villa-Cuesta, J. Cumbers, R. Lehmann, D. L. Jones, and M. Tatar . 2008. Drosophila germ-line modulation of insulin signaling and lifespan. Proc. Natl. Acad. Sci. USA 105:6368-6373.
21. Fournier-Level, A., A. M. Wilczek, M. D. Cooper, J. L. Roe, J. Anderson, D. Eaton, B. T. Moyers, R. H. Petipas, R. N. Schaeffer, B. Pieper, et al. 2013. Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana. Mol. Ecol 22:3552-3566.
22. Giannakou, M. E., and L. Partridge . 2007. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem. Sci. 32:180-188.
23. Gilchrist, G. W., and R. B. Huey . 2004. Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Integr. Comp. Biol. 44:461-470.
24. Grönke, S., D. F. Clarke, S. Broughton, T. D. Andrews, and L. Partridge . 2010. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLOS Genet. 6:e1000857.
25. Guirao-Rico, S., and M. Aguadé . 2009. Positive selection has driven the evolution of the Drosophila Insulin-like receptor (InR) at different timescales. Mol. Biol. Evol. 26:1723-1732.
26. Harshman, L. G., and A. J. Zera . 2007. The cost of reproduction: the devil in the details. Trends Ecol. Evol. 22:80-86.
27. Hoffmann, A. A., and L. G. Harshman . 1999. Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83:637-643.
28. Hoffmann, A. A., R. Hallas, C. Sinclair, and P. Mitrovski . 2001. Levels of variation in stress resistance in Drosophila among strains, local populations, and geographic regions: patterns for desiccation, starvation, cold resistance, and associated traits. Evolution 55:1621-1630.
29. Hoffmann, A. A., J. Shirriffs, and M. Scott . 2005. Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Funct. Ecol. 19:222-227.
30. Hoffmann, A. A., E. Ratna, C. M. Sgrò, M. Barton, M. Blacket, R. Hallas, S. De Garis, and A. R. Weeks . 2007. Antagonistic selection between adult thorax and wing size in field released Drosophila melanogaster independent of thermal conditions. J. Evol. Biol. 20:2219-2227.
31. Huey, R. B., G. W. Gilchrist, M. L. Carlson, D. Berrigan, and L. Serra . 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308-309.
32. Hwangbo, D. S., B. Gershman, M. P. Tu, M. Palmer, and M. Tatar . 2004. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body. Nature 429:562-566.
33. Jones, F. C., M. G. Grabherr, Y. F. Chan, P. Russell, E. Mauceli, J. Johnson, R. Swofford, M. Pirun, M. C. Zody, S. White, et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
34. Jovelin, R., J. S. Comstock, A. D. Cutter, and P. C. Phillips . 2014. A recent global selective sweep on the age-1 phosphatidylinositol 3-OH kinase regulator of the insulin-like signaling pathway within Caenorhabditis remanei. G3 4:1123-1133.
35. Jünger, M. A., F. Rintelen, H. Stocker, J. D. Wasserman, M. Vegh, T. Radimerski, M. E. Greenberg, and E. Hafen . 2003. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2:20.
36. Karan, D., A. K. Munjal, P. Gibert, B. Moreteau, R. Parkash, and J. R. David . 1998. Latitudinal clines for morphometrical traits in Drosophila kikkawai: a study of natural populations from the Indian subcontinent. Genet. Res. 71:31-38.
37. Khazaeli, A. A., and J. W. Curtsinger . 2010. Life history variation in an artificially selected population of Drosophila melanogaster: pleiotropy, superflies, and age-specific adaptation. Evolution 64:3409-3416.
38. Khazaeli, A. A., and J. W. Curtsinger. 2013. Pleiotropy and life history evolution in Drosophila melanogaster: uncoupling life span and early fecundity. J. Gerontol. A Biol. Sci. Med. Sci. 68:546-553.
39. Lee, S. F., Y. C. Eyre-Walker, R. V. Rane, C. Reuter, G. Vinti, L. Rako, L. Partridge, and A. A. Hoffmann . 2013. Polymorphism in the neurofibromin gene, Nf1, is associated with antagonistic selection on wing size and development time in Drosophila melanogaster. Mol. Ecol. 22:2716-2725.
40. Leroi, A. M., A. Bartke, G. De Benedictis, C. Franceschi, A. Gartner, E. S. Gonos, M. E. Fedei, T. Kivisild, S. Lee, N. Kartaf-Ozer, et al. 2005. What evidence is there for the existence of individual genes with antagonistic pleiotropic effects? Mech. Ageing Dev. 126:421-429.
41. Li, H., and R. Durbin . 2009. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
42. Linnen, C. R., Y. P. Poh, B. K. Peterson, R. D. Barrett, J. G. Larson, J. D. Jensen, and H. E. Hoekstra . 2013. Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339:1312-1316.
43. Mackay, T. F., S. Richards, E. A. Stone, A. Barbadilla, J. F. Ayroles, D. Zhu, S. Casillas, Y. Han, M. M. Magwire, J. M. Cridland, et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482:173-178.
44. Mattila, J., A. Bremer, L. Ahonen, R. Kostiainen, and O. Puig . 2009. Drosophila FoxO regulates organism size and stress resistance through an adenylate cyclase. Mol. Cell. Biol. 29:5357-5365.
45. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, K. Garimella, D. Altshuler, S. Gabriel, M. Daly, et al. 2010. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297-1303.
46. Méndez-Vigo, B., J. M. Martínez-Zapater, and C. Alonso-Blanco . 2013. The flowering repressor SVP underlies a novel Arabidopsis thaliana QTL interacting with the genetic background. PLOS Genet. 9:e1003289.
47. Mitrovski, P., and A. A. Hoffmann . 2001. Postponed reproduction as an adaptation to winter conditions in Drosophila melanogaster: evidence for clinal variation under semi-natural conditions. Proc. Biol. Sci. 268:2163-2168.
48. Paaby, A. B., and M. V. Rockman . 2013. The many faces of pleiotropy. Trends Genet. 29:66-73.
49. Paaby, A. B., and P. S. Schmidt . 2008. Functional significance of allelic variation at methuselah, an aging gene in Drosophila. PLOS One 3:e1987.
50. Paaby, A. B., and P. S. Schmidt. 2009. Dissecting the genetics of longevity in Drosophila melanogaster. Fly 3:29-38.
51. Paaby, A. B., M. J. Blacket, A. A. Hoffmann, and P. S. Schmidt . 2010. Identification of a candidate adaptive polymorphism for Drosophila life history by parallel independent clines on two continents. Mol. Ecol. 19:760-774.
52. Partridge, L., and D. Gems . 2002. The evolution of longevity. Curr. Biol. 12:R544-546.
53. Partridge, L., N. Prowse, and P. Pignatelli . 1999. Another set of responses and correlated responses to selection on age at reproduction in Drosophila melanogaster. Proc. Biol. Sci. 266:255-261.
54. Partridge, L., D. Gems, and D. J. Withers . 2005. Sex and death: what is the connection? Cell 120:461-472.
55. Puig, O., M. T. Marr, M. L. Ruhf, and R. Tjian . 2003. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17:2006-2020.
56. Rako, L., M. J. Blacket, S. W. McKechnie, and A. A. Hoffmann . 2007. Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Mol. Ecol. 16:2948-2957.
57. Remolina, S. C., P. L. Chang, J. Leips, S. V. Nuzhdin, and K. A. Hughes . 2012. Genomic basis of aging and life-history evolution in Drosophila melanogaster. Evolution 66:3390-3403.
58. Reznick, D. 1985. Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257-267.
59. Schmidt, P. S., and A. B. Paaby . 2008. Reproductive diapause and life-history clines in North American populations of Drosophila melanogaster. Evolution 62:1204-1215.
60. Schmidt, P. S., L. Matzkin, M. Ippolito, and W. F. Eanes . 2005a. Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59:1721-1732.
61. Schmidt, P. S., A. B. Paaby, and M. S. Heschel . 2005b. Genetic variance for diapause expression and associated life histories in Drosophila melanogaster. Evolution 59:2616-2625.
62. Schmidt, P. S., C. T. Zhu, J. Das, M. Batavia, L. Yang, and W. F. Eanes . 2008. An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 105:16207-16211.
63. Sgrò, C. M., B. van Heerwaarden, V. Kellermann, C. W. Wee, A. A. Hoffmann, and S. F. Lee . 2013. Complexity of the genetic basis of ageing in nature revealed by a clinal study of lifespan and methuselah, a gene for ageing, in Drosophila from eastern Australia. Mol. Ecol. 22:3539-3551.
64. Stearns, S. C. 1991. Trade-offs in life-history evolution. Funct. Ecol. 3:259-268.
65. Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, New York.
66. Stern, D. L. 2000. Evolutionary developmental biology and the problem of variation. Evolution 54:1079-1091.
67. Swindell, W. R., and J. L. Bouzat . 2006. Inbreeding depression and male survivorship in Drosophila: implications for senescence theory. Genetics 172:317-327.
68. Tatar, M., A. Kopelman, D. Epstein, M. P. Tu, C. M. Yin, and R. S. Garofalo . 2001. A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science 292:107-110.
69. Tatar, M., A. Bartke, and A. Antebi . 2003. The endocrine regulation of aging by insulin-like signals. Science 299:1346-1351.
70. Toivonen, J. M., and L. Partridge . 2009. Endocrine regulation of aging and reproduction in Drosophila. Mol. Cell Endocrinol. 299:39-50.
71. Trotta, V., F. C. Calboli, M. Ziosi, D. Guerra, M. C. Pezzoli, J. R. David, and S. Cavicchi . 2006. Thermal plasticity in Drosophila melanogaster: a comparison of geographic populations. BMC Evol. Biol. 6:67.
72. Vermeulen, C. J., and V. Loeschcke . 2007. Longevity and the stress response in Drosophila. Exp. Geront. 42:153-159.
73. Vihervaara, T., and O. Puig . 2008. dFOXO regulates transcription of a Drosophila acid lipase. J. Mol. Biol. 376:1215-1223.
74. Wang, M. C., D. Bohmann, and H. Jasper . 2005. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121:115-125.
75. Williams, G. C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398-411.