Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Retroviral restriction factor TRIM5α exhibits a high degree of sequence variation among primate species. It has been proposed that this diversity is the cumulative result of ancient, lineage-specific episodes of positive selection. Here, we describe the contribution of within-species variation to the evolution of TRIM5α. Sampling within two geographically distinct Old World monkey species revealed extensive polymorphism, including individual polymorphisms that predate speciation (shared polymorphism). In some instances, alleles were more closely related to orthologues of other species than to one another. Both silent and nonsynonymous changes clustered in two domains. Functional assays revealed consequences of polymorphism, including differential restriction of a small panel of retroviruses by very similar alleles. Together, these features indicate that the primate TRIM5α locus has evolved under balancing selection. Except for the MHC there are few, if any, examples of long-term balancing selection in primates. Our results suggest a complex evolutionary scenario, in which fixation of lineage-specific adaptations is superimposed on a subset of critical polymorphisms that predate speciation events and have been maintained by balancing selection for millions of years.

Bibliography

Newman, R. M., Hall, L., Connole, M., Chen, G.-L., Sato, S., Yuste, E., Diehl, W., Hunter, E., Kaur, A., Miller, G. M., & Johnson, W. E. (2006). Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5α. Proceedings of the National Academy of Sciences, 103(50), 19134–19139.

Authors 11
  1. Ruchi M. Newman (first)
  2. Laura Hall (additional)
  3. Michelle Connole (additional)
  4. Guo-Lin Chen (additional)
  5. Shuji Sato (additional)
  6. Eloisa Yuste (additional)
  7. William Diehl (additional)
  8. Eric Hunter (additional)
  9. Amitinder Kaur (additional)
  10. Gregory M. Miller (additional)
  11. Welkin E. Johnson (additional)
References 67 Referenced 138
  1. 10.1038/nature02343
  2. 10.1073/pnas.0402876101
  3. 10.1073/pnas.0409853102
  4. 10.1128/JVI.79.7.3930-3937.2005
  5. 10.1016/j.gene.2005.06.045
  6. 10.1016/j.molcel.2004.12.001
  7. 10.1038/nrmicro1248
  8. 10.1038/ni1125
  9. 10.1073/pnas.0402361101
  10. 10.1073/pnas.0402474101
  11. 10.1073/pnas.0403364101
  12. 10.1128/JVI.79.5.3139-3145.2005
  13. 10.1128/JVI.79.10.6111-6121.2005
  14. 10.1016/j.cub.2004.12.042
  15. 10.1128/JVI.79.14.8969-8978.2005
  16. 10.1093/emboj/20.9.2140
  17. 10.1074/jbc.M502145200
  18. 10.1128/JVI.79.22.14446-14450.2005
  19. 10.1016/j.virol.2006.05.017
  20. 10.1073/pnas.0509996103
  21. 10.1186/1742-4690-2-40
  22. 10.1128/JVI.79.1.176-183.2005
  23. 10.1128/JVI.78.21.12066-12070.2004
  24. 10.1073/pnas.0404640101
  25. 10.1128/JVI.78.10.5423-5437.2004
  26. JR Napier, PH Napier The Natural History of Primates (MIT Press, Cambridge, MA, 1985). / The Natural History of Primates by Napier JR (1985)
  27. 10.1146/annurev.iy.08.040190.003013
  28. 10.1038/ni1296
  29. 10.1111/j.1600-0684.1995.tb00155.x
  30. 10.1097/00002030-199007000-00002
  31. 10.1128/JVI.74.3.1209-1223.2000
  32. 10.1128/JVI.72.5.3872-3886.1998
  33. 10.1016/S1074-7613(03)00060-8
  34. 10.1111/j.1600-0684.2005.00122.x
  35. 10.1093/genetics/124.4.967
  36. 10.1073/pnas.94.15.7730
  37. 10.1016/j.jhevol.2004.11.007
  38. 10.1007/s10528-005-6777-z
  39. 10.1098/rstb.1995.0078
  40. 10.1073/pnas.200348197
  41. 10.1371/journal.pgen.0020064
  42. 10.1007/s002510050646
  43. 10.1128/JVI.75.11.5182-5188.2001
  44. 10.1128/JVI.74.16.7422-7430.2000
  45. 10.1128/JVI.80.5.2463-2471.2006
  46. 10.1016/j.cub.2005.11.045
  47. 10.1016/j.virol.2006.06.031
  48. 10.1186/1742-4690-3-54
  49. 10.1046/j.1365-294X.2000.01125.x
  50. 10.1016/S0169-5347(96)10051-3
  51. 10.1073/pnas.96.16.9172
  52. 10.1038/335167a0
  53. 10.1146/annurev.genet.32.1.415
  54. 10.1016/j.tig.2004.11.001
  55. 10.1007/BF00187453
  56. 10.1038/nature04655
  57. 10.1086/383092
  58. 10.1353/hub.2001.0075
  59. 10.1086/338304
  60. 10.1128/JVI.00283-06
  61. 10.1128/JVI.79.12.7883-7888.2005
  62. 10.1126/science.272.5258.67
  63. PB Medawar Retroviruses, eds JM Coffin, SH Hughes, HE Varmus (Cold Spring Harbor Lab Press, Plainview, NY, 1997). / Retroviruses by Medawar PB (1997)
  64. 10.1128/JVI.78.21.11715-11725.2004
  65. 10.1128/JVI.77.14.7779-7785.2003
  66. 10.1128/JVI.72.12.9597-9611.1998
  67. DL Swofford, paup*. Phylogenetic Analysis Using Parsimony (*and Other Methods) 4.0b10 (Sinauer Associates, Sunderland, MA, 2003). / Phylogenetic Analysis Using Parsimony (*and Other Methods) 4.0b10 by Swofford DL (2003)
Dates
Type When
Created 18 years, 9 months ago (Dec. 1, 2006, 8:34 p.m.)
Deposited 3 years, 4 months ago (April 12, 2022, 3:05 p.m.)
Indexed 3 weeks, 6 days ago (Aug. 6, 2025, 9:24 a.m.)
Issued 18 years, 8 months ago (Dec. 12, 2006)
Published 18 years, 8 months ago (Dec. 12, 2006)
Published Online 18 years, 8 months ago (Dec. 12, 2006)
Published Print 18 years, 8 months ago (Dec. 12, 2006)
Funders 0

None

@article{Newman_2006, title={Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5α}, volume={103}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0605838103}, DOI={10.1073/pnas.0605838103}, number={50}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Newman, Ruchi M. and Hall, Laura and Connole, Michelle and Chen, Guo-Lin and Sato, Shuji and Yuste, Eloisa and Diehl, William and Hunter, Eric and Kaur, Amitinder and Miller, Gregory M. and Johnson, Welkin E.}, year={2006}, month=dec, pages={19134–19139} }