Predictable phenotypic, but not karyotypic, evolution of populations with contrasting initial history

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Simões, Pedro ^a   Fragata, Inês ^a,d   Seabra, Sofia G ^a   Faria, Gonçalo S ^a,e   Santos, Marta A ^a,f   Rose, Michael R ^b   Santos, Mauro ^c   Matos, Margarida ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^d INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^e UNIVERSITY OF ST ANDREWS   (United Kingdom)

^f Nona Medical School   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BODY SIZE; DROSOPHILA; HUMAN; LATITUDE; LIFE HISTORY; NATURAL POPULATION; NONHUMAN; ADAPTATION; ANATOMY AND HISTOLOGY; ANIMAL; EUROPE; GENETIC SELECTION; GENETICS; KARYOTYPE; KARYOTYPING; MOLECULAR EVOLUTION; PHENOTYPE; PROCEDURES;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BODY SIZE; DROSOPHILA; EUROPE; EVOLUTION, MOLECULAR; KARYOTYPE; KARYOTYPING; PHENOTYPE; SELECTION, GENETIC;

EID: 85018423716     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-00968-1     Document Type: Article

References (67)

1. Orgogozo, V. Replaying the tape of life in the twenty-first century. Interface Focus 5, 20150057 (2015).
2. Lobkovsky, A. E. & Koonin, E. V. Replaying the tape of life: quantification of the predictability of evolution. Front. Genet. 3, 246 (2012).
3. Conte, G. L., Arnegard, M. E., Peichel, C. L. & Schluter, D. The probability of genetic parallelism and convergence in natural populations. Proc. R. Soc. B 279, 5039-5047 (2012).
4. Matos, M. et al. History, chance and selection during phenotypic and genomic experimental evolution: replaying the tape of life at different levels. Front. Genet. 6, 71 (2015).
5. Kawecki, T. J. et al. Experimental Evolution. Trends Ecol. Evol. 27, 547-560 (2012).
6. Lenski, R. E. & Travisano, M. Dynamics of adaptation and diversification: A 10, 000-generation experiment with bacterial populations. Proc. Natl. Acad. Sci. USA 91, 6808-6814 (1994).
7. Blount, Z. D., Barrick, J. E., Davidson, C. J. & Lenski, R. E. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature 489, 513-518 (2012).
8. Tenaillon, O. et al. The molecular diversity of adaptive convergence. Science 335, 457-461 (2012).
9. Tenaillon, O. et al. Tempo and mode of genome evolution in a 50, 000 generation experiment. Nature 536, 165-170 (2016).
10. Lachapelle, J., Reid, J. & Colegrave, N. Repeatability of adaptation in experimental populations of different sizes. Proc. R. Soc. B 282, 20143033 (2015).
11. Bailey, S. F., Rodrigue, N. & Kassen, R. The effect of selection environment on the probability of parallel evolution. Mol. Biol. Evol. 32, 1436-1448 (2015).
12. de Visser, J. A. G. M. & Krug, J. Empirical fitness landscapes and the predictability of evolution. Nat. Rev. Genet. 15, 480-490 (2014).
13. Blount, Z. D., Borland, C. Z. & Lenski, R. E. Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl. Acad. Sci. USA 105, 7899-7906 (2008).
14. Lenski, R. E. et al. Sustained fitness gains and variability in fitness trajectories in the long-Term evolution experiment with Escherichia coli. Proc. R. Soc. B 20152292 (2015).
15. Dettman, J. R. et al. Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Mol. Ecol 21, 2058-2077 (2012).
16. Long, A., Liti, G., Luptak, A. & Tenaillon, O. Elucidating the molecular architecture of adaptation via evolve and resequence experiments. Nat. Rev. Genet. 16, 567-582 (2015).
17. Cohan, F. M. & Hoffmann, A. A. Genetic divergence under uniform selection. II. Different responses to selection for knockdown resistance to ethanol among Drosophila melanogaster populations and their replicate lines. Genetics 114, 145-164 (1986).
18. Travisano, M., Mongold, J. A., Bennett, A. F. & Lenski, R. E. Experimental Tests of the Roles of Adaptation, Chance, and History in Evolution. Science 267, 87-90 (1995).
19. Teotónio, H. & Rose, M. R. Variation in the reversibility of evolution. Nature 408, 463-466 (2000).
20. Flatt, T. & Heyland, A. (eds.). Mechanisms of Life History Evolution. The Genetics and Physiology of Life History Traits and Trade-Offs. (Oxford University Press, 2011).
21. Melnyk, A. H. & Kassen, R. Adaptive landscapes in evolving populations of Pseudomonas fluorescens. Evolution 65, 3048-3059 (2011).
22. Spor, A. et al. Phenotypic and genotypic convergences are influenced by historical contingency and environment in yeast. Evolution 68, 772-790 (2014).
23. Bedhomme, S., Lafforgue, G. & Elena, S. F. Genotypic but not phenotypic historical contingency revealed by viral experimental evolution. BMC Evol. Biol. 13, 46 (2013).
24. Teotónio, H., Matos, M. & Rose, M. Reverse evolution of fitness in Drosophila melanogaster. J. Evol. Biol. 15, 608-617 (2002).
25. Joshi, A., Castillo, R. B. & Mueller, L. D. The contribution of ancestry, chance, and past and ongoing selection to adaptive evolution. J. Genet. 82, 147-162 (2003).
26. Fragata, I. et al. Laboratory selection quickly erases historical differentiation. PLoS One 9, e96227 (2014).
27. Fragata, I. et al. Keeping your options open: Maintenance of thermal plasticity during adaptation to a stable environment. Evolution 70, 195-206 (2016).
28. Simoes, P., Rose, M. R., Duarte, A., Gonçalves, R. & Matos, M. Evolutionary domestication in Drosophila subobscura. J. Evol. Biol 20, 758-766 (2007).
29. Simoes, P. et al. How repeatable is adaptive evolution? The role of geographical origin and founder effects in laboratory adaptation. Evolution 62, 1817-1829 (2008).
30. Teotónio, H., Chelo, I. M., Bradić, M., Rose, M. R. & Long, A. D. Experimental evolution reveals natural selection on standing genetic variation. Nat. Genet. 41, 251-257 (2009).
31. Hoffmann, A. A. & Rieseberg, L. H. Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? Annu. Rev. Ecol. Evol. Syst. 39, 21-42 (2008).
32. Rezende, E. et al. Climate change and chromosomal inversions in Drosophila subobscura. Clim. Res 43, 103-114 (2010).
33. Dobzhansky, T. Genetics of the Evolutionary Process. (Columbia University Press, 1970).
34. Kapun, M., Van Schalkwyk, H., McAllister, B., Flatt, T. & Schlötterer, C. Inference of chromosomal inversion dynamics from Pool-Seq data in natural and laboratory populations of Drosophila melanogaster. Mol. Ecol. 23, 1813-1827 (2014).
35. Fragata, I. et al. How much can history constrain adaptive evolution? A real-Time evolutionary approach of inversion polymorphisms in Drosophila subobscura. J. Evol. Biol. 27, 2727-2738 (2014).
36. Santos, J. et al. Tracking changes in chromosomal arrangements and their genetic content during adaptation. J. Evol. Biol. 29, 1151-1167 (2016).
37. Huey, R. B., Gilchrist, G. W., Carlson, M. L., Berrigan, D. & Serra, L. Rapid Evolution of a Geographic Cline in Size in an Introduced Fly. Science 287, 308-309 (2000).
38. Gilchrist, G. W., Huey, R. B., Balanya, J., Pascual, M. & Serra, L. A time series of evolution in action: A latitudinal cline in wing size in South American Drosophila subobscura. Evolution 58, 768-780 (2004).
39. Santos, J. et al. From nature to the laboratory: The impact of founder effects on adaptation. J. Evol. Biol. 25, 2607-2622 (2012).
40. Matos, M., Rose, M. R., Rocha Pité, M. T., Rego, C. & Avelar, T. Adaptation to the laboratory environment in Drosophila subobscura. J. Evol. Biol. 13, 9-19 (2000).
41. Balanya, J., Oller, J. M., Huey, R. B., Gilchrist, G. W. & Serra, L. Global genetic change tracks global climate warming in Drosophila subobscura. Science 313, 1773-1775 (2006).
42. Lenormand, T., Roze, D. & Rousset, F. Stochasticity in evolution. Trends Ecol. Evol. 24, 157-165 (2009).
43. Lefranc, A. & Bundgaard, J. The influence of male and female body size on copulation duration and fecundity in Drosophila melanogaster. Hereditas 132, 243-247 (2000).
44. Woods, R. E., Sgro, C. M., Hercus, M. J. & Hoffmann, A. A. Fluctuating asymmetry, fecundity and development time in Drosophila: Is there an association under optimal and stress conditions? J. Evol. Biol 15, 146-157 (2002).
45. Roff, D. A. & Mousseau, T. A. Quantitative genetics and fitness: lessons from Drosophila. Heredity 58, 103-118 (1987).
46. Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics. (Longmans Green, 1996).
47. Hoffmann, A. A. & Harshman, L. G. Desiccation and starvation resistance in Drosophila: patterns of variation at the species, population and intrapopulation levels. Heredity 83, 637-643 (1999).
48. Rion, S. & Kawecki, T. J. Evolutionary biology of starvation resistance: What we have learned from Drosophila. J. Evol. Biol. 20, 1655-1664 (2007).
49. Fragata, I. et al. Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura. J. Evol. Biol. 23, 112-123 (2010).
50. Simoes, P. et al. Wing trait-inversion associations in Drosophila subobscura can be generalized within continents, but may change through time. J. Evol. Biol. 28, 2163-2174 (2015).
51. Calabria, G. et al. Hsp70 protein levels and thermotolerance in Drosophila subobscura: A reassessment of the thermal co-Adaptation hypothesis. J. Evol. Biol. 25, 691-700 (2012).
52. Rego, C. et al. Clinal patterns of chromosomal inversion polymorphisms in Drosophila subobscura are partly associated with thermal preferences and heat stress resistance. Evolution 64, 385-397 (2010).
53. Santos, M., Tarrío, R., Zapata, C. & Alvarez, G. Sexual selection on chromosomal polymorphism in Drosophila subobscura. Heredity 57, 161-169 (1986).
54. Santos, M. Recombination load in a chromosomal inversion polymorphism of Drosophila subobscura. Genetics 181, 803-809 (2009).
55. Simoes, P., Calabria, G., Picao-Osório, J., Balanya, J. & Pascual, M. The genetic content of chromosomal inversions across a wide latitudinal gradient. PLoS One 7, e51625 (2012).
56. Pegueroles, C., Aquadro, C. F., Mestres, F. & Pascual, M. Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura. Heredity 110, 520-529 (2013).
57. Inoue, Y. The fate of polymorphic inversions of Drosophila melanogaster transferred to laboratory conditions. Japanese J. Genet. 54, 83-96 (1979).
58. Bailey, S. F., Blanquart, F., Bataillon, T. & Kassen, R. What drives parallel evolution? BioEssays 39, 1600176 (2016).
59. Barrett, R. D. H. & Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 23, 38-44 (2008).
60. Burke, M. et al. Genome-wide analysis of a long-Term evolution experiment with Drosophila. Nature 467, 587-590 (2010).
61. Burke, M. K., Liti, G. & Long, A. D. Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Mol. Biol. Evol. 31, 3228-3239 (2014).
62. Graves, J. L. Jr. et al. Genomics of Parallel Experimental Evolution in Drosophila. Mol. Biol. Evol. doi:10.1093/molbev/msw282 (2017).
63. Dryden, I. L. & Mardia, K. V. Statistical Shape Analysis. (John Wiley & Sons, 1998).
64. Kunze-Möhl, E. & Möller, E. Weitere Untersuchungen öber die chromosomale Struktur und die naturlichen Strukturtypen von Drosophila subobscura coll. Chromosoma 9, 559-570 (1957).
65. Lewis, P. & Zaykin, D. Genetic Data Analysis: computer program for analysis of allelic data, Version 1.1. Available from http://www. eeb.uconn.edu/people/ple (2001).
66. Landis, J. R., Heyman, E. R. & Koch, G. G. Average partial association in 3-way contingency tables: A review and discussion of alternative tests. Int. Stat. Rev. 46, 237-254 (1978).
67. Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165-1188 (2001).