The probability of genetic parallelism and convergence in natural populations

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1749, 2012, Pages 5039-5047

  Conte, Gina L ^a   Arnegard, Matthew E ^b   Peichel, Catherine L ^b   Schluter, Dolph ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b USA   (United States)

Author keywords

Convergent evolution; Genetic biases and constraints; Genetic convergence; Genetic parallelism; Genetics of adaptation; Parallel evolution

Indexed keywords

ADAPTATION; COMMON ANCESTRY; CONVERGENT EVOLUTION; PARALLEL EVOLUTION; PHENOTYPE; PROBABILITY;

EID: 84869116803     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2012.2146     Document Type: Review

References (63)

1. Endler, J. A. 1986 Natural selection in the wild. Princeton, NJ: Princeton University Press.
2. Harvey, P. H. & Pagel, M. D. 1991 The comparative method in evolutionary biology. Oxford, UK: Oxford University Press.
3. Schluter, D. 2000 The ecology of adaptive radiation. Oxford, UK: Oxford University Press.
4. Losos, J. B. 2011 Convergence, adaptation, and constraint. Evolution 65, 1827-1840. (doi:10.1111/J. 1558-5646.2011.01289.X)
5. Orr, H. A. 2005 The probability of parallel evolution. Evolution 59, 216-220. (doi:10.1111/j.0014-3820.2005. tb00907.x)
6. Weinreich, D. M., Delaney, N. F., DePristo, M. A. & Hartl, D. L. 2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312, 111-114. (doi:10.1126/science.1123539)
7. Gompel, N. & Prud'homme, B. 2009 The causes of repeated genetic evolution. Dev. Biol. 332, 36-47. (doi:10.1016/j.ydbio.2009.04.040)
8. Stern, D. L. & Orgogozo, V. 2009 Is genetic evolution predictable? Science 323, 746-751. (doi:10.1126/ science.1158997)
9. Chevin, L. M., Martin, G. & Lenormand, T. 2010 Fisher's model and the genomics of adaptation: restricted pleiotropy, heterogenous mutation, and parallel evolution. Evolution 64, 3213-3231. (doi:10.1111/j. 1558-5646.2010.01058.x)
10. Christin, P. A., Weinreich, D. M. & Besnard, G. 2010 Causes and evolutionary significance of genetic convergence. Trends Genet. 26, 400-405. (doi:10.1016/j.tig. 2010.06.005)
11. Streisfeld, M. A. & Rausher, M. D. 2011 Population genetics, pleiotropy, and the preferential fixation of mutations during adaptive evolution. Evolution 65, 629-642. (doi:10.1111/j.1558-5646.2010.01165.x)
12. Feldman, C. R., Brodie, E. D., Brodie, E. D. & Pfrender, M. E. 2012 Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proc. Natl Acad. Sci. USA 109, 4556-4561. (doi:10.1073/pnas. 1113468109)
13. Jost, M. C., Hillis, D. M., Lu, Y., Kyle, J. W., Fozzard, H. A. & Zakon, H. H. 2008 Toxin-resistant sodium channels: parallel adaptive evolution across a complete gene family. Mol. Biol. Evol. 25, 1016-1024. (doi:10.1093/ molbev/msn025)
14. Colosimo, P. F. et al. 2005 Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928-1933. (doi:10.1126/science. 1107239)
15. Knecht, A. K., Hosemann, K. E. & Kingsley, D. M. 2007 Constraints on utilization of the Eda-signaling pathway in threespine stickleback evolution. Evol. Dev. 9, 141-154. (doi:10.1111/j.1525-142X.2007.00145.x)
16. Wood, T. E., Burke, J.M. & Rieseberg, L. H. 2005 Parallel genotypic adaptation: when evolution repeats itself. Genetica 123, 157-170. (doi:10.1007/S10709-003-2738-9)
17. Arendt, J. & Reznick, D. 2008 Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26-32. (doi:10.1016/j.tree.2007.09.011)
18. Manceau, M., Domingues, V. S., Linnen, C. R., Rosenblum, E. B. & Hoekstra, H. E. 2010 Convergence in pigmentation at multiple levels: mutations, genes and function. Phil. Trans. R. Soc. B 365, 2439-2450. (doi:10.1098/rstb.2010.0104)
19. Elmer, K. R. & Meyer, A. 2011 Adaptation in the age of ecological genomics: insights from parallelism and convergence. Trends Ecol. Evol. 26, 298-306. (doi:10.1016/ j.tree.2011.02.008)
20. Turner, T. L., Bourne, E. C., Von Wettberg, E. J., Hu, T. T. & Nuzhdin, S. V. 2010 Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat. Genet. 42, 260-263. (doi:10.1038/ng.515)
21. Hancock, A.M. et al. 2010Human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proc. Natl Acad. Sci. USA 107(Suppl. 2), 8924-8930. (doi:10.1073/pnas.0914625107)
22. Jones, F. C. et al. 2012 The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55-61. (doi:10.1038/nature10944)
23. Chan, Y. F., Jones, F. C., McConnell, E., Bryk, J., Bunger, L. & Tautz, D. 2012 Parallel selection mapping using artificially selected mice reveals body weight control loci. Curr. Biol. 22, 1-7. (doi:10.1016/j.cub.2012.03.011)
24. Futuyma, D. J. 2009 Evolution, 2nd edn. Sunderland, MA: Sinauer Associates.
25. Campbell, D. & Bernatchez, L. 2004 Genomic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes. Mol. Biol. Evol. 21, 1164. (doi:10.1093/ molbev/msh153)
26. Bonin, A., Taberlet, P., Miaud, C. & Pompanon, F. 2006 Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol. Biol. Evol. 23, 773-783. (doi:10.1093/molbev/msj087)
27. Egan, S. P., Nosil, P. & Funk, D. J. 2008 Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62, 1162-1181. (doi:10.1111/j.1558-5646.2008.00352.x)
28. Hohenlohe, P. A., Bassham, S., Etter, P. D., Stiffler, N., Johnson, E. A. & Cresko, W. A. 2010 Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet. 6, e1000862. (doi:10.1371/journal.pgen.1000862)
29. Nosil, P., Egan, S. P. & Funk, D. J. 2008 Heterogeneous genomic differentiation between walking-stick ecotypes: 'Isolation by adaptation' and multiple roles for divergent selection. Evolution 62, 316-336. (doi:10.1111/j.1558-5646.2007.00299.x)
30. Bradbury, I. R. et al. 2010 Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature. Proc. R. Soc. B 277, 3725-3734. (doi:10.1098/rspb.2010.0985)
31. Papa, R. et al. 2008 Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies. BMC Genom. 9, 345. (doi:10.1186/1471-2164-9-345)
32. Baxter, S. W., Papa, R., Chamberlain, N., Humphray, S. J., Joron, M., Morrison, C., ffrench-Constant, R. H., McMillan, W. O. & Jiggins, C. D. 2008 Convergent evolution in the genetic basis of Mullerian mimicry in Heliconius butterflies. Genetics 180, 1567-1577. (doi:10. 1534/genetics.107.082982)
33. Reed, R. D. et al. 2011 Optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333, 1137-1141. (doi:10.1126/science.1208227)
34. Protas, M. E., Hersey, C., Kochanek, D., Zhou, Y., Wilkens, H., Jeffery, W. R., Zon, L. I., Borowsky, R. & Tabin, C. J. 2006 Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat. Genet. 38, 107-111. (doi:10.1038/ng1700)
35. Linnen, C. R., Kingsley, E. P., Jensen, J. D. & Hoekstra, H. E. 2009 On the origin and spread of an adaptive allele in deer mice. Science 325, 1095-1098. (doi:10.1126/ science.1175826)
36. Arnegard, M. E., Zwickl, D. J., Lu, Y. & Zakon, H. H. 2010 Old gene duplication facilitates origin and diversification of an innovative communication system twice. Proc. Natl Acad. Sci. USA 107, 22 172-22 177. (doi:10. 1073/pnas.1011803107)
37. Zakon, H. H., Lu, Y., Zwickl, D. J. & Hillis, D. M. 2006 Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc. Natl Acad. Sci. USA 103, 3675-3680. (doi:10.1073/pnas.0600160103)
38. Kao, K. C. & Sherlock, G. 2008 Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40, 1499-1504. (doi:10.1038/ng.280)
39. Woods, R., Schneider, D., Winkworth, C. L., Riley, M. A. & Lenski, R. E. 2006 Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc. Natl Acad. Sci. USA 103, 9107-9112. (doi:10. 1073/pnas.0602917103)
40. Tenaillon, O., Rodri{dotless}guez-Verdugo, A., Gaut, R. L., McDonald, P., Bennett, A. F., Long, A. D. & Gaut, B. S. 2012 The molecular diversity of adaptive convergence. Science 335, 457-461. (doi:10.1126/science.1212986)
41. Wittkopp, P. J., Williams, B. L., Selegue, J. E. & Carroll, S. B. 2003 Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. Proc. Natl Acad. Sci. USA 100, 1808-1813. (doi:10.1073/pnas. 0336368100)
42. Quillen, E. E., Bauchet, M., Bigham, A. W., Delgado-Burbano, M. E., Faust, F. X., Klimentidis, Y. C., Mao, X. Y., Stoneking, M. & Shriver, M. D. 2012 OPRM1 and EGFR contribute to skin pigmentation differences between indigenous Americans and Europeans. Hum. Genet. 131, 1073-1080. (doi:10.1007/S00439-011-1135-1)
43. Steiner, C. C., Rompler, H., Boettger, L. M., Schoneberg, T. & Hoekstra, H. E. 2009 The genetic basis of phenotypic convergence in beach mice: similar pigment patterns but different genes. Mol. Biol. Evol. 26, 35-45. (doi:10.1093/molbev/msn218)
44. Rosenblum, E. B., Rompler, H., Schoneberg, T. & Hoekstra, H. E. 2010 Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc. Natl Acad. Sci. USA 107, 2113-2117. (doi:10.1073/pnas.0911042107)
45. Gross, J. B., Borowsky, R. & Tabin, C. J. 2009 A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genet. 5, e1000326. (doi:10.1371/ journal.pgen.1000326)
46. Ritland, K., Newton, C. & Marshall, H. D. 2001 Inheritance and population structure of the white-phased 'Kermode' black bear. Curr. Biol. 11, 1468-1472. (doi:10.1016/S0960-9822(01)00448-1)
47. Theron, E., Hawkins, K., Bermingham, E., Ricklefs, R. E. & Mundy, N. I. 2001 The molecular basis of an avian plumage polymorphism in the wild: a melanocortin-1-receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba flaveola. Curr. Biol. 11, 550-557. (doi:10.1016/ S0960-9822(01)00158-0)
48. Eizirik, E., Yuhki, N., Johnson, W. E., Menotti-Raymond, M., Hannah, S. S. & O'Brien, S. J. 2003 Molecular genetics and evolution of melanism in the cat family. Curr. Biol. 13, 448-453. (doi:10.1016/ S0960-9822(03)00128-3)
49. Nachman, M. W., Hoekstra, H. E. & D'Agostino, S. L. 2003 The genetic basis of adaptive melanism in pocket mice. Proc. Natl Acad. Sci. USA 100, 5268-5273. (doi:10.1073/pnas.0421157100)
50. Mundy, N. I., Badcock, N. S., Hart, T., Scribner, K., Janssen, K. & Nadeau, N. J. 2004 Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303, 1870-1873. (doi:10.1126/science. 1093834)
51. Rompler, H., Rohland, N., Lalueza-Fox, C., Willerslev, E., Kuznetsova, T., Rabeder, G., Bertranpetit, J., Schoneberg, T. & Hofreiter, M. 2006 Nuclear gene indicates coat-color polymorphism in mammoths. Science 313, 62. (doi:10.1126/science.1128994)
52. Hedges, S. B., Dudley, J. & Kumar, S. 2006 TIMETREE: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971-2972. (doi:10.1093/ bioinformatics/btl505)
53. Lavoue, S., Miya, M., Arnegard, M. E., Sullivan, J. P., Hopkins, C. D. & Nishida, M. 2012 Comparable ages for the independent origins of electrogenesis in African and South American weakly electric fishes. PLoS ONE 7, e36287. (doi:10.1371/journal.pone. 0036287)
54. Whittaker, R. H. 1952 A study of summer foliage insect communities in the Great Smoky Mountains. Ecol. Monogr. 22, 2-44. (doi:10.2307/1948527)
55. Pianka, E. R. 1973 The structure of lizard communities. Annu. Rev. Ecol. Syst. 4, 53-74. (doi:10.1146/annurev. es.04.110173.000413)
56. McCullagh, P. & Nelder, J. A. 1989 Generalized linear models, 2nd edn. London, UK: Chapman and Hall.
57. Barrett, R. D. H. & Schluter, D. 2008 Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44. (doi:10.1016/j.tree.2007.09.008)
58. Zhang, J. Z. 2003 Parallel functional changes in the digestive RNAses of ruminants and colobines by divergent amino acid substitutions. Mol. Biol. Evol. 20, 1310-1317. (doi:10.1093/molbev/msg143)
59. Roelants, K., Fry, B. G., Norman, J. A., Clynen, E., Schoofs, L. & Bossuyt, F. 2010 Identical skin toxins by convergent molecular adaptation in frogs. Curr. Biol. 20, 125-130. (doi:10.1016/j.cub.2009.11.015)
60. Zhang, J. Z. 2006 Parallel adaptive origins of digestive RNAses in Asian and African leaf monkeys. Nat. Genet. 38, 819-823. (doi:10.1038/ng1812)
61. Cooley, A. M. & Willis, J. H. 2009 Genetic divergence causes parallel evolution of flower color in Chilean Mimulus. New Phytol. 183, 729-739. (doi:10.1111/j. 1469-8137.2009.02858.x)
62. Cooley, A. M., Modliszewski, J. L., Rommel, M. L. & Willis, J. H. 2011 Gene duplication in Mimulus underlies parallel floral evolution via independent trans-regulatory changes. Curr. Biol. 21, 700-704. (doi:10.1016/j.cub. 2011.03.028)
63. Stern, D. L. & Orgogozo, V. 2008 The loci of evolution: how predictable is genetic evolution? Evolution 62, 2155-2177. (doi:10.1111/j.1558-5646. 2008.00450.x)