Disentangling genetic and epigenetic determinants of ultrafast adaptation
Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an...
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| Autor*in: |
Gjuvsland, Arne B [verfasserIn] Zörgö, Enikö [verfasserIn] Samy, Jeevan KA [verfasserIn] Stenberg, Simon [verfasserIn] Demirsoy, Ibrahim H [verfasserIn] Roque, Francisco [verfasserIn] Maciaszczyk‐Dziubinska, Ewa [verfasserIn] Migocka, Magdalena [verfasserIn] Alonso‐Perez, Elisa [verfasserIn] Zackrisson, Martin [verfasserIn] Wysocki, Robert [verfasserIn] Tamás, Markus J [verfasserIn] Jonassen, Inge [verfasserIn] Omholt, Stig W [verfasserIn] Warringer, Jonas [verfasserIn] |
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| Format: |
E-Artikel |
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| Sprache: |
Englisch |
| Erschienen: |
2016 |
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| Schlagwörter: |
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| Anmerkung: |
© The Author(s) 2016 |
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| Übergeordnetes Werk: |
Enthalten in: Molecular Systems Biology - Nature Publishing Group UK, 2023, 12(2016), 12 vom: 15. Dez. |
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| Übergeordnetes Werk: |
volume:12 ; year:2016 ; number:12 ; day:15 ; month:12 |
| Links: |
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| DOI / URN: |
10.15252/msb.20166951 |
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| Katalog-ID: |
SPR058092145 |
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| 520 | |a Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. | ||
| 520 | |a Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. | ||
| 520 | |a Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. | ||
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| 700 | 1 | |a Zörgö, Enikö |e verfasserin |4 aut | |
| 700 | 1 | |a Samy, Jeevan KA |e verfasserin |4 aut | |
| 700 | 1 | |a Stenberg, Simon |e verfasserin |4 aut | |
| 700 | 1 | |a Demirsoy, Ibrahim H |e verfasserin |0 (orcid)0000-0001-7825-7787 |4 aut | |
| 700 | 1 | |a Roque, Francisco |e verfasserin |4 aut | |
| 700 | 1 | |a Maciaszczyk‐Dziubinska, Ewa |e verfasserin |4 aut | |
| 700 | 1 | |a Migocka, Magdalena |e verfasserin |4 aut | |
| 700 | 1 | |a Alonso‐Perez, Elisa |e verfasserin |4 aut | |
| 700 | 1 | |a Zackrisson, Martin |e verfasserin |4 aut | |
| 700 | 1 | |a Wysocki, Robert |e verfasserin |4 aut | |
| 700 | 1 | |a Tamás, Markus J |e verfasserin |4 aut | |
| 700 | 1 | |a Jonassen, Inge |e verfasserin |4 aut | |
| 700 | 1 | |a Omholt, Stig W |e verfasserin |4 aut | |
| 700 | 1 | |a Warringer, Jonas |e verfasserin |0 (orcid)0000-0001-6144-2740 |4 aut | |
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10.15252/msb.20166951 doi (DE-627)SPR058092145 (SPR)msb.20166951-e DE-627 ger DE-627 rakwb eng Gjuvsland, Arne B verfasserin (orcid)0000-0002-4391-3411 aut Disentangling genetic and epigenetic determinants of ultrafast adaptation 2016 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2016 Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 Zörgö, Enikö verfasserin aut Samy, Jeevan KA verfasserin aut Stenberg, Simon verfasserin aut Demirsoy, Ibrahim H verfasserin (orcid)0000-0001-7825-7787 aut Roque, Francisco verfasserin aut Maciaszczyk‐Dziubinska, Ewa verfasserin aut Migocka, Magdalena verfasserin aut Alonso‐Perez, Elisa verfasserin aut Zackrisson, Martin verfasserin aut Wysocki, Robert verfasserin aut Tamás, Markus J verfasserin aut Jonassen, Inge verfasserin aut Omholt, Stig W verfasserin aut Warringer, Jonas verfasserin (orcid)0000-0001-6144-2740 aut Enthalten in Molecular Systems Biology Nature Publishing Group UK, 2023 12(2016), 12 vom: 15. Dez. (DE-627)490536905 (DE-600)2193510-5 1744-4292 nnns volume:12 year:2016 number:12 day:15 month:12 https://dx.doi.org/10.15252/msb.20166951 X:SPRINGER Resolving-System kostenfrei Volltext SYSFLAG_0 GBV_SPRINGER GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_72 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_171 GBV_ILN_206 GBV_ILN_213 GBV_ILN_224 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_636 GBV_ILN_2001 GBV_ILN_2003 GBV_ILN_2004 GBV_ILN_2005 GBV_ILN_2006 GBV_ILN_2007 GBV_ILN_2009 GBV_ILN_2010 GBV_ILN_2011 GBV_ILN_2014 GBV_ILN_2015 GBV_ILN_2020 GBV_ILN_2021 GBV_ILN_2025 GBV_ILN_2026 GBV_ILN_2027 GBV_ILN_2034 GBV_ILN_2037 GBV_ILN_2038 GBV_ILN_2044 GBV_ILN_2048 GBV_ILN_2049 GBV_ILN_2050 GBV_ILN_2055 GBV_ILN_2056 GBV_ILN_2057 GBV_ILN_2059 GBV_ILN_2061 GBV_ILN_2064 GBV_ILN_2068 GBV_ILN_2088 GBV_ILN_2093 GBV_ILN_2106 GBV_ILN_2108 GBV_ILN_2110 GBV_ILN_2111 GBV_ILN_2118 GBV_ILN_2122 GBV_ILN_2129 GBV_ILN_2143 GBV_ILN_2144 GBV_ILN_2147 GBV_ILN_2148 GBV_ILN_2152 GBV_ILN_2153 GBV_ILN_2190 GBV_ILN_2232 GBV_ILN_2336 GBV_ILN_2470 GBV_ILN_2507 GBV_ILN_2522 GBV_ILN_2548 GBV_ILN_4012 GBV_ILN_4029 GBV_ILN_4035 GBV_ILN_4037 GBV_ILN_4046 GBV_ILN_4112 GBV_ILN_4116 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4155 GBV_ILN_4242 GBV_ILN_4246 GBV_ILN_4249 GBV_ILN_4251 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4311 GBV_ILN_4313 GBV_ILN_4314 GBV_ILN_4315 GBV_ILN_4318 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4326 GBV_ILN_4328 GBV_ILN_4333 GBV_ILN_4334 GBV_ILN_4335 GBV_ILN_4336 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4393 GBV_ILN_4598 GBV_ILN_4700 AR 12 2016 12 15 12 |
| spelling |
10.15252/msb.20166951 doi (DE-627)SPR058092145 (SPR)msb.20166951-e DE-627 ger DE-627 rakwb eng Gjuvsland, Arne B verfasserin (orcid)0000-0002-4391-3411 aut Disentangling genetic and epigenetic determinants of ultrafast adaptation 2016 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2016 Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 Zörgö, Enikö verfasserin aut Samy, Jeevan KA verfasserin aut Stenberg, Simon verfasserin aut Demirsoy, Ibrahim H verfasserin (orcid)0000-0001-7825-7787 aut Roque, Francisco verfasserin aut Maciaszczyk‐Dziubinska, Ewa verfasserin aut Migocka, Magdalena verfasserin aut Alonso‐Perez, Elisa verfasserin aut Zackrisson, Martin verfasserin aut Wysocki, Robert verfasserin aut Tamás, Markus J verfasserin aut Jonassen, Inge verfasserin aut Omholt, Stig W verfasserin aut Warringer, Jonas verfasserin (orcid)0000-0001-6144-2740 aut Enthalten in Molecular Systems Biology Nature Publishing Group UK, 2023 12(2016), 12 vom: 15. Dez. (DE-627)490536905 (DE-600)2193510-5 1744-4292 nnns volume:12 year:2016 number:12 day:15 month:12 https://dx.doi.org/10.15252/msb.20166951 X:SPRINGER Resolving-System kostenfrei Volltext SYSFLAG_0 GBV_SPRINGER GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_72 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_171 GBV_ILN_206 GBV_ILN_213 GBV_ILN_224 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_636 GBV_ILN_2001 GBV_ILN_2003 GBV_ILN_2004 GBV_ILN_2005 GBV_ILN_2006 GBV_ILN_2007 GBV_ILN_2009 GBV_ILN_2010 GBV_ILN_2011 GBV_ILN_2014 GBV_ILN_2015 GBV_ILN_2020 GBV_ILN_2021 GBV_ILN_2025 GBV_ILN_2026 GBV_ILN_2027 GBV_ILN_2034 GBV_ILN_2037 GBV_ILN_2038 GBV_ILN_2044 GBV_ILN_2048 GBV_ILN_2049 GBV_ILN_2050 GBV_ILN_2055 GBV_ILN_2056 GBV_ILN_2057 GBV_ILN_2059 GBV_ILN_2061 GBV_ILN_2064 GBV_ILN_2068 GBV_ILN_2088 GBV_ILN_2093 GBV_ILN_2106 GBV_ILN_2108 GBV_ILN_2110 GBV_ILN_2111 GBV_ILN_2118 GBV_ILN_2122 GBV_ILN_2129 GBV_ILN_2143 GBV_ILN_2144 GBV_ILN_2147 GBV_ILN_2148 GBV_ILN_2152 GBV_ILN_2153 GBV_ILN_2190 GBV_ILN_2232 GBV_ILN_2336 GBV_ILN_2470 GBV_ILN_2507 GBV_ILN_2522 GBV_ILN_2548 GBV_ILN_4012 GBV_ILN_4029 GBV_ILN_4035 GBV_ILN_4037 GBV_ILN_4046 GBV_ILN_4112 GBV_ILN_4116 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4155 GBV_ILN_4242 GBV_ILN_4246 GBV_ILN_4249 GBV_ILN_4251 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4311 GBV_ILN_4313 GBV_ILN_4314 GBV_ILN_4315 GBV_ILN_4318 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4326 GBV_ILN_4328 GBV_ILN_4333 GBV_ILN_4334 GBV_ILN_4335 GBV_ILN_4336 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4393 GBV_ILN_4598 GBV_ILN_4700 AR 12 2016 12 15 12 |
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10.15252/msb.20166951 doi (DE-627)SPR058092145 (SPR)msb.20166951-e DE-627 ger DE-627 rakwb eng Gjuvsland, Arne B verfasserin (orcid)0000-0002-4391-3411 aut Disentangling genetic and epigenetic determinants of ultrafast adaptation 2016 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2016 Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 Zörgö, Enikö verfasserin aut Samy, Jeevan KA verfasserin aut Stenberg, Simon verfasserin aut Demirsoy, Ibrahim H verfasserin (orcid)0000-0001-7825-7787 aut Roque, Francisco verfasserin aut Maciaszczyk‐Dziubinska, Ewa verfasserin aut Migocka, Magdalena verfasserin aut Alonso‐Perez, Elisa verfasserin aut Zackrisson, Martin verfasserin aut Wysocki, Robert verfasserin aut Tamás, Markus J verfasserin aut Jonassen, Inge verfasserin aut Omholt, Stig W verfasserin aut Warringer, Jonas verfasserin (orcid)0000-0001-6144-2740 aut Enthalten in Molecular Systems Biology Nature Publishing Group UK, 2023 12(2016), 12 vom: 15. Dez. (DE-627)490536905 (DE-600)2193510-5 1744-4292 nnns volume:12 year:2016 number:12 day:15 month:12 https://dx.doi.org/10.15252/msb.20166951 X:SPRINGER Resolving-System kostenfrei Volltext SYSFLAG_0 GBV_SPRINGER GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_72 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_171 GBV_ILN_206 GBV_ILN_213 GBV_ILN_224 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_636 GBV_ILN_2001 GBV_ILN_2003 GBV_ILN_2004 GBV_ILN_2005 GBV_ILN_2006 GBV_ILN_2007 GBV_ILN_2009 GBV_ILN_2010 GBV_ILN_2011 GBV_ILN_2014 GBV_ILN_2015 GBV_ILN_2020 GBV_ILN_2021 GBV_ILN_2025 GBV_ILN_2026 GBV_ILN_2027 GBV_ILN_2034 GBV_ILN_2037 GBV_ILN_2038 GBV_ILN_2044 GBV_ILN_2048 GBV_ILN_2049 GBV_ILN_2050 GBV_ILN_2055 GBV_ILN_2056 GBV_ILN_2057 GBV_ILN_2059 GBV_ILN_2061 GBV_ILN_2064 GBV_ILN_2068 GBV_ILN_2088 GBV_ILN_2093 GBV_ILN_2106 GBV_ILN_2108 GBV_ILN_2110 GBV_ILN_2111 GBV_ILN_2118 GBV_ILN_2122 GBV_ILN_2129 GBV_ILN_2143 GBV_ILN_2144 GBV_ILN_2147 GBV_ILN_2148 GBV_ILN_2152 GBV_ILN_2153 GBV_ILN_2190 GBV_ILN_2232 GBV_ILN_2336 GBV_ILN_2470 GBV_ILN_2507 GBV_ILN_2522 GBV_ILN_2548 GBV_ILN_4012 GBV_ILN_4029 GBV_ILN_4035 GBV_ILN_4037 GBV_ILN_4046 GBV_ILN_4112 GBV_ILN_4116 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4155 GBV_ILN_4242 GBV_ILN_4246 GBV_ILN_4249 GBV_ILN_4251 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4311 GBV_ILN_4313 GBV_ILN_4314 GBV_ILN_4315 GBV_ILN_4318 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4326 GBV_ILN_4328 GBV_ILN_4333 GBV_ILN_4334 GBV_ILN_4335 GBV_ILN_4336 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4393 GBV_ILN_4598 GBV_ILN_4700 AR 12 2016 12 15 12 |
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10.15252/msb.20166951 doi (DE-627)SPR058092145 (SPR)msb.20166951-e DE-627 ger DE-627 rakwb eng Gjuvsland, Arne B verfasserin (orcid)0000-0002-4391-3411 aut Disentangling genetic and epigenetic determinants of ultrafast adaptation 2016 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2016 Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 Zörgö, Enikö verfasserin aut Samy, Jeevan KA verfasserin aut Stenberg, Simon verfasserin aut Demirsoy, Ibrahim H verfasserin (orcid)0000-0001-7825-7787 aut Roque, Francisco verfasserin aut Maciaszczyk‐Dziubinska, Ewa verfasserin aut Migocka, Magdalena verfasserin aut Alonso‐Perez, Elisa verfasserin aut Zackrisson, Martin verfasserin aut Wysocki, Robert verfasserin aut Tamás, Markus J verfasserin aut Jonassen, Inge verfasserin aut Omholt, Stig W verfasserin aut Warringer, Jonas verfasserin (orcid)0000-0001-6144-2740 aut Enthalten in Molecular Systems Biology Nature Publishing Group UK, 2023 12(2016), 12 vom: 15. Dez. (DE-627)490536905 (DE-600)2193510-5 1744-4292 nnns volume:12 year:2016 number:12 day:15 month:12 https://dx.doi.org/10.15252/msb.20166951 X:SPRINGER Resolving-System kostenfrei Volltext SYSFLAG_0 GBV_SPRINGER GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_72 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_171 GBV_ILN_206 GBV_ILN_213 GBV_ILN_224 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_636 GBV_ILN_2001 GBV_ILN_2003 GBV_ILN_2004 GBV_ILN_2005 GBV_ILN_2006 GBV_ILN_2007 GBV_ILN_2009 GBV_ILN_2010 GBV_ILN_2011 GBV_ILN_2014 GBV_ILN_2015 GBV_ILN_2020 GBV_ILN_2021 GBV_ILN_2025 GBV_ILN_2026 GBV_ILN_2027 GBV_ILN_2034 GBV_ILN_2037 GBV_ILN_2038 GBV_ILN_2044 GBV_ILN_2048 GBV_ILN_2049 GBV_ILN_2050 GBV_ILN_2055 GBV_ILN_2056 GBV_ILN_2057 GBV_ILN_2059 GBV_ILN_2061 GBV_ILN_2064 GBV_ILN_2068 GBV_ILN_2088 GBV_ILN_2093 GBV_ILN_2106 GBV_ILN_2108 GBV_ILN_2110 GBV_ILN_2111 GBV_ILN_2118 GBV_ILN_2122 GBV_ILN_2129 GBV_ILN_2143 GBV_ILN_2144 GBV_ILN_2147 GBV_ILN_2148 GBV_ILN_2152 GBV_ILN_2153 GBV_ILN_2190 GBV_ILN_2232 GBV_ILN_2336 GBV_ILN_2470 GBV_ILN_2507 GBV_ILN_2522 GBV_ILN_2548 GBV_ILN_4012 GBV_ILN_4029 GBV_ILN_4035 GBV_ILN_4037 GBV_ILN_4046 GBV_ILN_4112 GBV_ILN_4116 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4155 GBV_ILN_4242 GBV_ILN_4246 GBV_ILN_4249 GBV_ILN_4251 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4311 GBV_ILN_4313 GBV_ILN_4314 GBV_ILN_4315 GBV_ILN_4318 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4326 GBV_ILN_4328 GBV_ILN_4333 GBV_ILN_4334 GBV_ILN_4335 GBV_ILN_4336 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4393 GBV_ILN_4598 GBV_ILN_4700 AR 12 2016 12 15 12 |
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10.15252/msb.20166951 doi (DE-627)SPR058092145 (SPR)msb.20166951-e DE-627 ger DE-627 rakwb eng Gjuvsland, Arne B verfasserin (orcid)0000-0002-4391-3411 aut Disentangling genetic and epigenetic determinants of ultrafast adaptation 2016 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier © The Author(s) 2016 Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 Zörgö, Enikö verfasserin aut Samy, Jeevan KA verfasserin aut Stenberg, Simon verfasserin aut Demirsoy, Ibrahim H verfasserin (orcid)0000-0001-7825-7787 aut Roque, Francisco verfasserin aut Maciaszczyk‐Dziubinska, Ewa verfasserin aut Migocka, Magdalena verfasserin aut Alonso‐Perez, Elisa verfasserin aut Zackrisson, Martin verfasserin aut Wysocki, Robert verfasserin aut Tamás, Markus J verfasserin aut Jonassen, Inge verfasserin aut Omholt, Stig W verfasserin aut Warringer, Jonas verfasserin (orcid)0000-0001-6144-2740 aut Enthalten in Molecular Systems Biology Nature Publishing Group UK, 2023 12(2016), 12 vom: 15. Dez. (DE-627)490536905 (DE-600)2193510-5 1744-4292 nnns volume:12 year:2016 number:12 day:15 month:12 https://dx.doi.org/10.15252/msb.20166951 X:SPRINGER Resolving-System kostenfrei Volltext SYSFLAG_0 GBV_SPRINGER GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_31 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_72 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_171 GBV_ILN_206 GBV_ILN_213 GBV_ILN_224 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_636 GBV_ILN_2001 GBV_ILN_2003 GBV_ILN_2004 GBV_ILN_2005 GBV_ILN_2006 GBV_ILN_2007 GBV_ILN_2009 GBV_ILN_2010 GBV_ILN_2011 GBV_ILN_2014 GBV_ILN_2015 GBV_ILN_2020 GBV_ILN_2021 GBV_ILN_2025 GBV_ILN_2026 GBV_ILN_2027 GBV_ILN_2034 GBV_ILN_2037 GBV_ILN_2038 GBV_ILN_2044 GBV_ILN_2048 GBV_ILN_2049 GBV_ILN_2050 GBV_ILN_2055 GBV_ILN_2056 GBV_ILN_2057 GBV_ILN_2059 GBV_ILN_2061 GBV_ILN_2064 GBV_ILN_2068 GBV_ILN_2088 GBV_ILN_2093 GBV_ILN_2106 GBV_ILN_2108 GBV_ILN_2110 GBV_ILN_2111 GBV_ILN_2118 GBV_ILN_2122 GBV_ILN_2129 GBV_ILN_2143 GBV_ILN_2144 GBV_ILN_2147 GBV_ILN_2148 GBV_ILN_2152 GBV_ILN_2153 GBV_ILN_2190 GBV_ILN_2232 GBV_ILN_2336 GBV_ILN_2470 GBV_ILN_2507 GBV_ILN_2522 GBV_ILN_2548 GBV_ILN_4012 GBV_ILN_4029 GBV_ILN_4035 GBV_ILN_4037 GBV_ILN_4046 GBV_ILN_4112 GBV_ILN_4116 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4155 GBV_ILN_4242 GBV_ILN_4246 GBV_ILN_4249 GBV_ILN_4251 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4311 GBV_ILN_4313 GBV_ILN_4314 GBV_ILN_4315 GBV_ILN_4318 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4326 GBV_ILN_4328 GBV_ILN_4333 GBV_ILN_4334 GBV_ILN_4335 GBV_ILN_4336 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4393 GBV_ILN_4598 GBV_ILN_4700 AR 12 2016 12 15 12 |
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Enthalten in Molecular Systems Biology 12(2016), 12 vom: 15. Dez. volume:12 year:2016 number:12 day:15 month:12 |
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Gjuvsland, Arne B @@aut@@ Zörgö, Enikö @@aut@@ Samy, Jeevan KA @@aut@@ Stenberg, Simon @@aut@@ Demirsoy, Ibrahim H @@aut@@ Roque, Francisco @@aut@@ Maciaszczyk‐Dziubinska, Ewa @@aut@@ Migocka, Magdalena @@aut@@ Alonso‐Perez, Elisa @@aut@@ Zackrisson, Martin @@aut@@ Wysocki, Robert @@aut@@ Tamás, Markus J @@aut@@ Jonassen, Inge @@aut@@ Omholt, Stig W @@aut@@ Warringer, Jonas @@aut@@ |
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This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general.</subfield></datafield><datafield tag="520" ind1=" " ind2=" "><subfield code="a">Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components.</subfield></datafield><datafield tag="520" ind1=" " ind2=" "><subfield code="a">Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables.</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">adaptation</subfield><subfield code="7">(dpeaa)DE-He213</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">epigenetics</subfield><subfield code="7">(dpeaa)DE-He213</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">evolution</subfield><subfield code="7">(dpeaa)DE-He213</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">modelling</subfield><subfield code="7">(dpeaa)DE-He213</subfield></datafield><datafield tag="650" ind1=" " ind2="4"><subfield code="a">population genetics</subfield><subfield code="7">(dpeaa)DE-He213</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Zörgö, Enikö</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Samy, Jeevan KA</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Stenberg, Simon</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Demirsoy, Ibrahim H</subfield><subfield code="e">verfasserin</subfield><subfield code="0">(orcid)0000-0001-7825-7787</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Roque, Francisco</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Maciaszczyk‐Dziubinska, Ewa</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Migocka, Magdalena</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Alonso‐Perez, Elisa</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Zackrisson, Martin</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Wysocki, Robert</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Tamás, Markus J</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Jonassen, Inge</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Omholt, Stig W</subfield><subfield code="e">verfasserin</subfield><subfield code="4">aut</subfield></datafield><datafield tag="700" ind1="1" ind2=" "><subfield code="a">Warringer, Jonas</subfield><subfield code="e">verfasserin</subfield><subfield code="0">(orcid)0000-0001-6144-2740</subfield><subfield code="4">aut</subfield></datafield><datafield tag="773" ind1="0" ind2="8"><subfield code="i">Enthalten in</subfield><subfield code="t">Molecular Systems Biology</subfield><subfield code="d">Nature Publishing Group UK, 2023</subfield><subfield code="g">12(2016), 12 vom: 15. 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Gjuvsland, Arne B misc adaptation misc epigenetics misc evolution misc modelling misc population genetics Disentangling genetic and epigenetic determinants of ultrafast adaptation |
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Disentangling genetic and epigenetic determinants of ultrafast adaptation adaptation (dpeaa)DE-He213 epigenetics (dpeaa)DE-He213 evolution (dpeaa)DE-He213 modelling (dpeaa)DE-He213 population genetics (dpeaa)DE-He213 |
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Disentangling genetic and epigenetic determinants of ultrafast adaptation |
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Gjuvsland, Arne B Zörgö, Enikö Samy, Jeevan KA Stenberg, Simon Demirsoy, Ibrahim H Roque, Francisco Maciaszczyk‐Dziubinska, Ewa Migocka, Magdalena Alonso‐Perez, Elisa Zackrisson, Martin Wysocki, Robert Tamás, Markus J Jonassen, Inge Omholt, Stig W Warringer, Jonas |
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disentangling genetic and epigenetic determinants of ultrafast adaptation |
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Disentangling genetic and epigenetic determinants of ultrafast adaptation |
| abstract |
Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. © The Author(s) 2016 |
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Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. © The Author(s) 2016 |
| abstract_unstemmed |
Abstract A major rationale for the advocacy of epigenetically mediated adaptive responses is that they facilitate faster adaptation to environmental challenges. This motivated us to develop a theoretical–experimental framework for disclosing the presence of such adaptation‐speeding mechanisms in an experimental evolution setting circumventing the need for pursuing costly mutation–accumulation experiments. To this end, we exposed clonal populations of budding yeast to a whole range of stressors. By growth phenotyping, we found that almost complete adaptation to arsenic emerged after a few mitotic cell divisions without involving any phenotypic plasticity. Causative mutations were identified by deep sequencing of the arsenic‐adapted populations and reconstructed for validation. Mutation effects on growth phenotypes, and the associated mutational target sizes were quantified and embedded in data‐driven individual‐based evolutionary population models. We found that the experimentally observed homogeneity of adaptation speed and heterogeneity of molecular solutions could only be accounted for if the mutation rate had been near estimates of the basal mutation rate. The ultrafast adaptation could be fully explained by extensive positive pleiotropy such that all beneficial mutations dramatically enhanced multiple fitness components in concert. As our approach can be exploited across a range of model organisms exposed to a variety of environmental challenges, it may be used for determining the importance of epigenetic adaptation‐speeding mechanisms in general. Synopsis A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. We developed an integrated experimental–theoretical framework capable of evaluating transient and sustained genetic and epigenetic contributions to fast adaptation.The fastest adaptation we observed could be explained by classic neo‐Darwinistic mechanisms.Ultrafast adaptation emerged as a near‐deterministic consequence of positively pleiotropic mutations that simultaneously enhanced multiple fitness components. Graphical Abstract A novel theoretical–experimental framework is used to show that even in the case of ultrafast adaptation to an environmental stressor, there is no need to invoke epigenetic mechanisms as explanatory variables. © The Author(s) 2016 |
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Disentangling genetic and epigenetic determinants of ultrafast adaptation |
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Zörgö, Enikö Samy, Jeevan KA Stenberg, Simon Demirsoy, Ibrahim H Roque, Francisco Maciaszczyk‐Dziubinska, Ewa Migocka, Magdalena Alonso‐Perez, Elisa Zackrisson, Martin Wysocki, Robert Tamás, Markus J Jonassen, Inge Omholt, Stig W Warringer, Jonas |
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Zörgö, Enikö Samy, Jeevan KA Stenberg, Simon Demirsoy, Ibrahim H Roque, Francisco Maciaszczyk‐Dziubinska, Ewa Migocka, Magdalena Alonso‐Perez, Elisa Zackrisson, Martin Wysocki, Robert Tamás, Markus J Jonassen, Inge Omholt, Stig W Warringer, Jonas |
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10.15252/msb.20166951 |
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2024-10-25T04:55:59.036Z |
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| score |
7.401582 |