TY - JOUR
T1 - The rate and potential relevance of new mutations in a colonizing plant lineage
AU - Exposito-Alonso, Moises
AU - Becker, Claude
AU - Schuenemann, Verena J.
AU - Reiter, Ella
AU - Setzer, Claudia
AU - Slovak, Radka
AU - Brachi, Benjamin
AU - Hagmann, Jörg
AU - Grimm, Dominik G.
AU - Chen, Jiahui
AU - Busch, Wolfgang
AU - Bergelson, Joy
AU - Ness, Rob W.
AU - Krause, Johannes
AU - Burbano, Hernán A.
AU - Weigel, Detlef
N1 - Funding Information:
This study was supported by the President’s Fund of the Max Planck Society (project “Darwin”) to HAB and by an ERC grant (AdG IMMUNEMESIS) and core funds of the Max Planck Society to DW. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. For providing and retrieving herbarium specimens, we thank R. Capers, J. Devos, G. Shirsekar, M. S. Dossmann, J. Freudenstein, C. M. Herring, C. Niezgoda, C. A. McCormick, J. Peter and M. Thines. We thank X. Zhao and I. Henderson for recombination estimates, C. Lanz for sequencing support, C. Goeschl, B. Zierfuss and B. Wohlrab for help with root analyses, and P. Lang, D. Seymour, and D. Koenig for thorough proofreading and comments on the manuscript. We thank R. Colautti for useful comments on the theoretical framing of the manuscript, M. Nordborg for discussions and pointing us to the work of A.R. Templeton, K. Pruefer for input on data analysis, and D. Tautz, T. Mackay and the Weigel and Burbano labs for comments on the manuscript.
Publisher Copyright:
© 2018 Exposito-Alonso et al.
PY - 2018/2
Y1 - 2018/2
N2 - By following the evolution of populations that are initially genetically homogeneous, much can be learned about core biological principles. For example, it allows for detailed studies of the rate of emergence of de novo mutations and their change in frequency due to drift and selection. Unfortunately, in multicellular organisms with generation times of months or years, it is difficult to set up and carry out such experiments over many generations. An alternative is provided by “natural evolution experiments” that started from colonizations or invasions of new habitats by selfing lineages. With limited or missing gene flow from other lineages, new mutations and their effects can be easily detected. North America has been colonized in historic times by the plant Arabidopsis thaliana, and although multiple intercrossing lineages are found today, many of the individuals belong to a single lineage, HPG1. To determine in this lineage the rate of substitutions—the subset of mutations that survived natural selection and drift–, we have sequenced genomes from plants collected between 1863 and 2006. We identified 73 modern and 27 herbarium specimens that belonged to HPG1. Using the estimated substitution rate, we infer that the last common HPG1 ancestor lived in the early 17thcentury, when it was most likely introduced by chance from Europe. Mutations in coding regions are depleted in frequency compared to those in other portions of the genome, consistent with purifying selection. Nevertheless, a handful of mutations is found at high frequency in present-day populations. We link these to detectable phenotypic variance in traits of known ecological importance, life history and growth, which could reflect their adaptive value. Our work showcases how, by applying genomics methods to a combination of modern and historic samples from colonizing lineages, we can directly study new mutations and their potential evolutionary relevance.
AB - By following the evolution of populations that are initially genetically homogeneous, much can be learned about core biological principles. For example, it allows for detailed studies of the rate of emergence of de novo mutations and their change in frequency due to drift and selection. Unfortunately, in multicellular organisms with generation times of months or years, it is difficult to set up and carry out such experiments over many generations. An alternative is provided by “natural evolution experiments” that started from colonizations or invasions of new habitats by selfing lineages. With limited or missing gene flow from other lineages, new mutations and their effects can be easily detected. North America has been colonized in historic times by the plant Arabidopsis thaliana, and although multiple intercrossing lineages are found today, many of the individuals belong to a single lineage, HPG1. To determine in this lineage the rate of substitutions—the subset of mutations that survived natural selection and drift–, we have sequenced genomes from plants collected between 1863 and 2006. We identified 73 modern and 27 herbarium specimens that belonged to HPG1. Using the estimated substitution rate, we infer that the last common HPG1 ancestor lived in the early 17thcentury, when it was most likely introduced by chance from Europe. Mutations in coding regions are depleted in frequency compared to those in other portions of the genome, consistent with purifying selection. Nevertheless, a handful of mutations is found at high frequency in present-day populations. We link these to detectable phenotypic variance in traits of known ecological importance, life history and growth, which could reflect their adaptive value. Our work showcases how, by applying genomics methods to a combination of modern and historic samples from colonizing lineages, we can directly study new mutations and their potential evolutionary relevance.
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U2 - 10.1371/journal.pgen.1007155
DO - 10.1371/journal.pgen.1007155
M3 - Article
C2 - 29432421
AN - SCOPUS:85043343540
VL - 14
JO - PLoS Genetics
JF - PLoS Genetics
SN - 1553-7390
IS - 2
M1 - e1007155
ER -