title: 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 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.
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway arne.gjuvsland@nmbu.no jonas.warringer@cmb.gu.se.
authors.forename: Arne B
authors.identifier: http://orcid.org/0000-0002-4391-3411
authors.initials: AB
authors.lastname: Gjuvsland
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.|Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Enikö
authors.initials: E
authors.lastname: Zörgö
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
authors.forename: Jeevan Ka
authors.initials: JK
authors.lastname: Samy
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway.
authors.forename: Simon
authors.initials: S
authors.lastname: Stenberg
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Ibrahim H
authors.identifier: http://orcid.org/0000-0001-7825-7787
authors.initials: IH
authors.lastname: Demirsoy
authors.affiliation: Computational Biology Unit, University of Bergen, Bergen, Norway.
authors.forename: Francisco
authors.initials: F
authors.lastname: Roque
authors.affiliation: Institute of Experimental Biology, University of Wroclaw, Wroclaw, Poland.
authors.forename: Ewa
authors.initials: E
authors.lastname: Maciaszczyk-Dziubinska
authors.affiliation: Institute of Experimental Biology, University of Wroclaw, Wroclaw, Poland.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Migocka
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Elisa
authors.initials: E
authors.lastname: Alonso-Perez
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Martin
authors.initials: M
authors.lastname: Zackrisson
authors.affiliation: Institute of Experimental Biology, University of Wroclaw, Wroclaw, Poland.
authors.forename: Robert
authors.initials: R
authors.lastname: Wysocki
authors.affiliation: Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Markus J
authors.initials: MJ
authors.lastname: Tamás
authors.affiliation: Computational Biology Unit, University of Bergen, Bergen, Norway.
authors.forename: Inge
authors.initials: I
authors.lastname: Jonassen
authors.affiliation: Centre for Biodiversity Dynamics, Department of Biology, NTNU - Norwegian University of Science and Technology, Trondheim, Norway.
authors.forename: Stig W
authors.initials: SW
authors.lastname: Omholt
authors.affiliation: Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway arne.gjuvsland@nmbu.no jonas.warringer@cmb.gu.se.|Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden.
authors.forename: Jonas
authors.identifier: http://orcid.org/0000-0001-6144-2740
authors.initials: J
authors.lastname: Warringer
mesh_terms: D000222:Adaptation, Physiological; D001151:Arsenic / Q000494:pharmacology*; D001426:Bacterial Proteins / Q000235:genetics*; D044127:Epigenesis, Genetic; D019143:Evolution, Molecular; D056084:Genetic Fitness; D059014:High-Throughput Nucleotide Sequencing; D008957:Models, Genetic; D009154:Mutation; D004718:Saccharomycetales / Q000187:drug effects / Q000235:genetics / Q000254:growth & development*; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D049490:Systems Biology / Q000379:methods
chemical_list: D001426:Bacterial Proteins; D001151:Arsenic
keywords: adaptation; epigenetics; evolution; modelling; population genetics