Fitness effects of mutation in natural populations of Arabidopsis thaliana reveal a complex influence of local adaptation.
Fisher's geometric model
MA lines
mutational effect
mutational variance
mutations
standing genetic variation
Journal
Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
16
01
2020
revised:
21
08
2020
accepted:
13
09
2020
pubmed:
20
12
2020
medline:
5
10
2021
entrez:
19
12
2020
Statut:
ppublish
Résumé
Little is empirically known about the contribution of mutations to fitness in natural environments. However, Fisher's Geometric Model (FGM) provides a conceptual foundation to consider the influence of the environment on mutational effects. To quantify mutational properties in the field, we established eight sets of MA lines (7-10 generations) derived from eight founders collected from natural populations of Arabidopsis thaliana from French and Swedish sites, representing the range margins of the species in Europe. We reciprocally planted the MA lines and their founders at French and Swedish sites, allowing us to test predictions of FGM under naturally occurring environmental conditions. The performance of the MA lines relative to each other and to their respective founders confirmed some and contradicted other predictions of the FGM: the contribution of mutation to fitness variance increased when the genotype was in an environment where its fitness was low, that is, in the away environment, but mutations were more likely to be beneficial when the genotype was in its home environment. Consequently, environmental context plays a large role in the contribution of mutations to the evolutionary process and local adaptation does not guarantee that a genotype is at or close to its optimum.
Banques de données
Dryad
['10.5061/dryad.12jm63xx2']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
330-348Informations de copyright
© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.
Références
Abbott, R., and M. Gomes. 1989. Population genetic structure and outcrossing rate of Arabidopsis thaliana (L.) Heynh. Heredity 62:411-418.
Agrawal, A. F., and M. C. Whitlock. 2010. Environmental duress and epistasis: How does stress affect the strength of selection on new mutations? Trends Ecol. Evol 25:450-458.
Ågren, J., and D. W. Schemske. 2012. Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range. New Phytologist 194:1112-1122.
Ågren, J., C. G. Oakley, J. K. McKay, J. T. Lovell, and D. W. Schemske. 2013. Genetic mapping of adaptation reveals fitness trade-offs in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 110:21077-21082.
Ågren, J., C. G. Oakley, S. Lundemo, and D. W. Schemske. 2017. Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping. Evolution 71:550-564.
Bataillon, T. 2003. Shaking the ‘deleterious mutations’ dogma? Trends Ecol. Evol 18:315-317. https://doi.org/10.1016/S0169-5347(03)00128-9
Bataillon, T., T. Zhang, and R. Kassen. 2011. Cost of adaptation and fitness effects of beneficial mutations in pseudomonas fluorescens. Genetics 189:939-949. https://doi.org/10.1534/genetics.111.130468
Bates, D., M. Maechler, B. Bolker, and S. Walker. 2015. Fitting Linear Mixed-Effects Models Using lme4. Journal of Statistical Software 67:1-48.
Bomblies, K., L. Yant, R. A. Laitinen RA, S.-T. Kim, J. D. Hollister, N. Warthmann, J. Fitz, and D. Weigel. 2010. Local-scale patterns of genetic variability, outcrossing, and spatial structure in natural stands of Arabidopsis thaliana. PLoS Genetics 6:e1000890. https://doi.org/10.1371/journal.pgen.1000890
Böndel, K. B., S. A. Kraemer, T. S. Samuels, D. McClean, J. Lachapelle, R. W. Ness, N. Colegrave, and P. D. Keightley. 2019. Direct inference of the distribution of fitness effects of spontaneous mutations in Chlamydomonas reinhardtii. PLoS Biology 17: p. e3000192.
Burch, L. C., and L. Chao. 2000. Evolvability of an RNA virus determined by its mutational neighborhood. Nature 406:625-628.
Connallon, T., and A. G. Clark. 2014. Balancing Selection in Species with Separate Sexes: Insights from Fisher's Geometric Model. Genetics 197:991-1006. https://doi.org/10.1534/genetics.114.165605
Cotto, O., and O. Ronce. 2014. Maladaptation as a source of senescence in habitats variable in space and time. Evolution 68:2481-2493. https://doi.org/10.1111/evo.12462.
Exposito-Alonso, M., C. Becker, V. J. Schuenemann, E. Reiter, C. Setzer, R. Slovak, B. Brachi, J. Hagmann, D. G. Grimm, J. Chen, et al. 2018. The rate and potential relevance of new mutations in a colonizing plant lineage. PLOS Genetics 14:e1007155. https://doi.org/10.1371/journal.pgen.1007155
Eyre-Walker, A., and P. D. Keightley. 2007. The distribution of fitness effects of new mutations. Nat. Rev. Genet 8:610-618.
Exposito-Alonso, M., C. Becker, V. J. Schuenemann, E. Reiter, C. Setzer, R. Slovak, R. B. Brachi, J. HJagmann, D. G. Grimm, W. Busch, et al. 2018. The rate and potential relevance of new mutations in a colonizing plant lineage. PLoS Genet 14:e1007155. https://doi.org/10.1371/journal.pgen.1007155
Fisher, R. A. 1930. The genetical theory of natural selection. Oxford Univ. Press, Oxford, U.K.
Fenster, C. B., and L. Galloway. 1997. Developmental homeostasis: Evolutionary Consequences and Genetic Basis. International Journal of Plant Sciences S158:S121-S130.
Fournier-Level, A., A. Korte, M. D. Cooper, M. Nordborg, J. Schmitt, and A. M. Wilczek. 2011. A map of local adaptation in Arabidopsis thaliana. Science 334:86-89. https://doi.org/10.1126/science.1209271.
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, and M. Reymond. 2013. Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana. Molecular ecology 22:3552-3566. https://doi.org/10.1111/mec.12285.
Gifford, D. R., E. Moss, and R. C. Maclean. 2016. Environmental variation alters the fitness effects of rifampicin resistance mutations in Pseudomonas aeruginosa. Evolution 70:725-730. https://doi.org/10.1111/evo.12880
Hadfield, J. D. 2010. MCMC Methods for Multi-Response Generalized Linear Mixed Models: The MCMCglmm R Package. Journal of Statistical Software 33:1-22.
Hall, A. R. 2013. Genotype-by-environment interactions due to antibiotic resistance and adaptation in Escherichia coli. J Evol Biol 26:1655-1664. https://doi.org/10.1111/jeb.12172
Hall, D. W., R. Mahmoudizad, A. W. Hurd, and S. B. Joseph. 2008. Spontaneous mutations in diploid Saccharomyces cerevisiae: another thousand cell generations. Genet. Res 90:229-241.
Halligan, D. L., and P. D. Keightley. 2009. Spontaneous mutation accumulation studies in evolutionary genetics. Annual Reviews of Ecology, Evolution and Systematics 40:151-172. https://doi.org/10.1146/annurev.ecolsys.39.110707.173437
Hamilton, J. A., M. Okada, T. Korves, and J. Schmitt. 2015. The role of climate adaptation in colonization success in Arabidopsis thaliana. Molecular Ecology 24:2253-2263. https://doi.org/10.1111/mec.13099
Harmand, N., R. Gallet, R. Jabbour-Zahab, G. Martin, and T. Lenormand. 2017. Fisher's geometrical model and the mutational patterns of antibiotic resistance across dose gradients. Evolution 71:23-37. https://doi.org/10.1111/evo.13111
Hietpas, R. T., C. Bank, J. D. Jensen, and D. N. A. Bolon. 2013. Shifting fitness landscapes in response to altered environments. Evolution 67:3512-3522. https://doi.org/10.1111/evo.12207
Hoffmann, M. H., J. Tomiuk, H. Schmuths, C. Koch, and K. Bachmann. 2005. Phenological and morphological responses to different temperature treatments differ among a world-wide sample of accessions of Arabidopsis thaliana. Acta Oecologica 28:181-187.
Houle, D., B. Morikawa, and M. Lynch. 1996. Comparing mutational variabilities. Genetics 143:1467-1483.
Hubbard, A. T. M., N. V. Jafari, N. Feasey, J. L. Rohn, and A. P. Roberts. 2019. Effect of environment on the evolutionary trajectories and growth characteristics of antibiotic-resistant Escherichia coli mutants. Front. Microbiol 10:2001.
Hutchinson, G. E. 1965. The ecological theater and the evolutionary play. Yale Univ. Press, New Haven, CT.
Keightley, P. D., and M. Lynch. 2003. Towards a realistic model of mutations affecting fitness. Evolution 57:683-685.
Kondrashov, A. S., and D. Houle. 1994. Genotype-environment interactions and the estimation of the genomic mutation-rate in Drosophila melanogaster. Proc. R. Soc. Lond. B 258:221-227.
Lenormand, T., and M. Raymond. 1998. Resistance management: the stable zone strategy. Proceedings of the Royal Society of London. Series B: Biological Sciences 265:1985-1990.
Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Inc., Sunderland, MA.
Mackay, T. F. C., R. F. Lyman, M. S. Jackson, C. Terzian, and W. G. Hill. 1992. Polygenic mutation in Drosophila melanogaster: Estimates from divergence among inbred strains. Evolution 46:300-316.
Mackay, T. F. C., J. D. Fry, R. F. Lyman, and S. V. Nuzhdin. 1994. Polygenic mutation in Drosophila melanogaster: Estimates from response to selection of inbred strains. Genetics 136:937-951.
MacKenzie, J. L., F. E. Saade, Q. H. Le, T. E. Bureau, and D. J. Schoen. 2005. Genomic mutation in lines of Arabidopsis thaliana exposed to ultraviolet-B radiation. Genetics 171:715-723.
McKay, J. H., J. H. Richards, and T. Mitchell-Olds. 2003. Genetics of drought adaptation in Arabidopsis thaliana: I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology 12:1137-1151.
Martin, G., and T. Lenormand. 2006a. A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution 60:893-907.
Martin, G., and T. Lenormand. 2006b. The fitness effects of mutations across environments: a survey in light of fitness landscape models. Evolution 60:2413-2427.
Martin, G., and T. Lenormand. 2015. The fitness effect of mutations across environments: Fisher's geometrical model with multiple optima. Evolution 69:1433-1447. https://doi.org/10.1111/evo.12671
Muller, H. J. 1950. Evidence of the precision of genetic adaptation. Harvey Lecture Series 43:165-229.
Nei, M. 2013. Mutation-driven evolution. Oxford University Press, Oxford, UK.
Oakley, C. G., J. Ågren, R. A. Atchison, and D. W. Schemske. 2014. QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. Molecular Ecology 23:4304-4215.
Orr, H. A. 1998. The Population Genetics of Adaptation: The Distribution of Factors Fixed during Adaptive. Evolution 52:935-949.
Ossowski, S., K. Schneeberger, J. I. Lucas-Lledó, N. Warthmann, R. M. Clark, R. G. Shaw, D. Weigel, and M. Lynch. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:92-94.
Parsons, P. A. 1987. Evolutionary rates under environmental stress. In: M. K. Hecht, B. Wallace, G. T. Prance (eds) Evolutionary Biology. Springer, Boston, MA.
Perfeito, L., L. Fernandes, C. Mota, and I. Gordo. 2007. Adaptive mutations in bacteria: High rate and small effects. Science 317:813-815. https://doi.org/10.1126/science.1142284
Perfeito, L., A. Sousa, T. Bataillon, and I. Gordo. 2014. Rates of fitness decline and rebound suggest pervasive epistasis. Evolution 68:150-162. https://doi.org/10.1111/evo.12234
Pico, F. X., B. Mendez-Vigo, J. M. Martinez-Zapater, and C. Alonso-Blanco. 2008. Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian Peninsula. Genetics 180:1009-1021. https://doi.org/10.1534/genetics.108.089581
Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R.re. Team. 2018. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3. 1-137.
Polechová, J., N. Barton, and G. Marion. 2009. Species' range: adaptation in space and time. Am. Nat 174:E186-204. https://doi.org/10.1086/605958.
Platt, A., M. Horton, Y. S. Huang, Y. Li, A. E. Anastasio, N. W. Mulyati, J. Ågren, O. Bossdorf, D. Byers, K. Donohue, et al. 2010. The scale of population structure in Arabidopsis thaliana. PLOS Genetics 6:e1000843. https://doi.org/10.1371/journal.pgen.1000843
Postma, F. M., and J. Ågren. 2016. Early life stages contribute strongly to local adaptation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA 113:7590-7595.
Price, M., B. T. Moyers, L. Lopez, J. R. Lasky, J. G. Monroe, J. L. Mullen, C. G. Oakley, J. Lin, J. Ågren, D. R. Schrider, et al. 2018. Combining population genomics and fitness QTLs to identify the genetics of local adaptation in Arabidopsis thaliana. PNAS 115:5028-5033. https://doi.org/10.1073/pnas.1719998115
R-Core Team. 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Remold, S. K., and R. E. Lenski. 2001. Contribution of individual random mutations to genotype-by-environment interactions in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A 98:11388-11393.
Roles, A. J., M. T. Rutter, I. Dworkin, C. B. Fenster, and J. K. Conner. 2016. Field measurements of genotype by environment interaction for fitness caused by spontaneous mutation in Arabidopsis thaliana. Evolution 70:1039-1050. https://doi.org/10.1111/evo.12913
Rutter, M. T., and C. B. Fenster. 2007. Testing for adaptation to climate in Arabidopsis thaliana: A calibrated common garden approach. Annals of Botany 99:529-536. https://doi.org/10.1093/aob/mcl282
Rutter, M. T., F. H. Shaw, and C. B. Fenster. 2010. Spontaneous mutation parameters for Arabidopsis thaliana measured in the wild. Evolution 64:1825-1835. https://doi.org/10.1111/j.1558-5646.2009.00928.x
Rutter, M. T., A. Roles, J. Conner, R. Shaw, F. Shaw, K. Schneeberger, S. Ossowski, D. Weigel, and C. B. Fenster. 2012. Brief Communication: Fitness of Arabidopsis thaliana mutation accumulation lines whose spontaneous mutations are known. Evolution 66:2335-2339.
Rutter, M. T., Y. M. Wieckowski, C. J. Murren, and A. Strand. 2017. Fitness effects of mutation: Testing genetic redundancy in Arabidopsis thaliana. Journal of Evolutionary Biology 30:1124-1135. https://doi.org/10.1111/jeb.13081
Rutter, M. T., A. J. Roles, and C. B. Fenster. 2018. Quantifying natural seasonal variation in mutation parameters with mutation accumulation lines. Ecology and Evolution 8:5575-5585. https://doi.org/10.1002/ece3.4085
Samis, K. E., C. J. Murren, O. Bossdorf, K. Donohue, C. B. Fenster, R. L. Malmberg, M. D. Purugganan, and J. R. Stinchcombe. 2012. Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana. Ecology and Evolution 2:1162-1180.
SAS 9.4. 2019. SAS Institute, Cary NC.
Schaack, S., D. E. Allen, L. C. Latta IV, K. K. Morgan, and M. Lynch. 2013. Short Communication: The effect of spontaneous mutations on competitive ability. J . Evol. Biol 26:451-456.
Shaw, R. G., D. L. Byers, and E. Darmo. 2000. Spontaneous mutational effects on reproductive traits of Arabidopsis thaliana. Genetics 155:369-378.
Shaw, F. H., C. J. Geyer, and R. G. Shaw. 2002. A comprehensive model of mutations affecting fitness and inferences for Arabidopsis thaliana. Evolution 56:453-463.
Schoen, D. J., and S. T. Schultz. 2019. Somatic mutation and evolution in plants. Annu. Rev. Ecol. Evol. Syst 50:2.1-2.25. https://doi.org/10.1146/annurev-ecolsys-110218-024955
Silander, O. K., O. Tenaillon, and L. Chao. 2007. Understanding the evolutionary fate of finite populations: the dynamics of mutational effects. PloS Biol 5:922-931.
Somssich, M. 2019. A short history of Arabidopsis thaliana (L.) Heynh. Columbia-0. Peerj Preprints, https://doi.org/10.7287/peerj.preprints.26931v5
Stearns, F. W., and C. B. Fenster. 2016. The effect of induced mutations on quantitative traits in Arabidopsis thaliana: Natural versus artificial conditions. Ecology and Evolution 6:8366-8374. https://doi.org/10.1002/ece3.2558
Stenøien, H. K., C. B. Fenster, H. Kuittinen, and O. Savolainen. 2002. Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae). Amer. J. Bot 89:1604-1608.
Stenøien, H. K., C. B. Fenster, A. Tonteri, and O. Savolainen. 2005. High genetic variability in natural populations of Arabidopsis thaliana from Northern Europe. Molecular Ecology 14:137-148.
Stinchcombe, J. R., C. Weinig, M. Ungerer M, K. M. Olsen KM, C. Mays, S. S. Halldorsdottir, M. D. Purugganan, and J. Schmitt. 2004. A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences of the USA 101:4712-4717.
Thiergart, T., P. Duran, T. Ellis, R. Garrido-Oter, N. Vannier, E. Kemen, F. Roux, C. Alonso-Blanco, J. Ågren, P. Schulze-Lefert, et al. 2020. Root microbiota assembly and adaptive differentiation among European Arabidopsis populations. Nature Ecology and Evolution 4:122-131.
Timoféeff-Ressovsky, N. W. 1940. Mutations and geographical variation. In: The new systematics, ed. J. S. Huxley, pp: 73-136. Oxford University Press, Oxford.
Tonsor, S. J., T. W. Elnaccash, and S. M. Scheiner. 2013. Developmental instability is genetically correlated with phenotypic plasticity, constraining heritability, and fitness. Evolution 67:2923-2935.
Urbina, H., M. F. Breed, W. Zhao, K. Lakshmi-Gurrala, S. G. E. Andersson, J. Å gren, S. Baldauf, and A. Rosling. 2018. Specificity in Arabidopsis thaliana recruitment of root fungal communities from soil and rhizosphere. Fungal Biol 122:231-240. https://doi.org/10.1016/j.funbio.2017.12.013.
Vale, P. F., M. Choisy, R. Froissart, R. Sanjuán, and S. Gandon. 2012. The distribution of mutational fitness effects of phage φX174 on different hosts. Evolution 66:3495-3507. https://doi.org/10.1111/j.1558-5646.2012.01691.x
Wang, A. D., N. P. Sharp, C. C. Spencer, K. Tedman-Aucoin, and A. F. Agrawal. 2009. Selection, Epistasis, and Parent-of-Origin Effects on Deleterious Mutations across Environments in Drosophila melanogaster. The American Naturalist 174:863-874. https://doi.org/10.1086/645088
Weng, M.-L., C. Becker, J. Hildebrandt, M. Rutter, R. Shaw, D. Weigel, and C. B. Fenster. 2019. Fine-grained analyses of spontaneous mutation spectrum and frequency in Arabidopsis thaliana. Genetics 211:703-714. https://doi.org/10.1534/genetics.118.301721
Zhang, M., P. Azad, and R. C. Woodruff. 2011. Adaptation of Drosophila melanogaster to increased NaCl concentration due to dominant beneficial mutations. Genetica 139:177-186. https://doi.org/10.1007/s10709-010-9535-z.