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Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast

Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this...

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Autores principales: Kroll, Evgueny, Coyle, Scott, Dunn, Barbara, Koniges, Gregory, Aragon, Anthony, Edwards, Jeremy, Rosenzweig, Frank
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3722211/
https://www.ncbi.nlm.nih.gov/pubmed/23894280
http://dx.doi.org/10.1371/journal.pone.0066414
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author Kroll, Evgueny
Coyle, Scott
Dunn, Barbara
Koniges, Gregory
Aragon, Anthony
Edwards, Jeremy
Rosenzweig, Frank
author_facet Kroll, Evgueny
Coyle, Scott
Dunn, Barbara
Koniges, Gregory
Aragon, Anthony
Edwards, Jeremy
Rosenzweig, Frank
author_sort Kroll, Evgueny
collection PubMed
description Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this phenomenon are typically carried out under benign conditions, which result in low rates of genetic change unlikely to initiate reproductive isolation. Previously, we described an experimental system using the yeast Saccharomyces cerevisiae where starvation served as a proxy to any stress that decreases reproduction and/or survivorship. We showed that novel lineages with restructured genomes quickly emerged in starved populations, and that these survivors were more fit than their ancestors when re-starved. Here we show that certain yeast lineages that survive starvation have become reproductively isolated from their ancestor. We further demonstrate that reproductive isolation arises from genomic rearrangements, whose frequency in starving yeast is several orders of magnitude greater than an unstarved control. By contrast, the frequency of point mutations is less than 2-fold greater. In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome. We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility. This type of reproductive barrier, whether arising spontaneously or via genetic manipulation, can be removed by making a lineage euploid for the altered chromosomes. Our model provides direct genetic evidence that reproductive isolation can arise frequently in stressed populations via genome restructuring without the precondition of geographic isolation.
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spelling pubmed-37222112013-07-26 Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast Kroll, Evgueny Coyle, Scott Dunn, Barbara Koniges, Gregory Aragon, Anthony Edwards, Jeremy Rosenzweig, Frank PLoS One Research Article Knowledge of the mechanisms that lead to reproductive isolation is essential for understanding population structure and speciation. While several models have been advanced to explain post-mating reproductive isolation, experimental data supporting most are indirect. Laboratory investigations of this phenomenon are typically carried out under benign conditions, which result in low rates of genetic change unlikely to initiate reproductive isolation. Previously, we described an experimental system using the yeast Saccharomyces cerevisiae where starvation served as a proxy to any stress that decreases reproduction and/or survivorship. We showed that novel lineages with restructured genomes quickly emerged in starved populations, and that these survivors were more fit than their ancestors when re-starved. Here we show that certain yeast lineages that survive starvation have become reproductively isolated from their ancestor. We further demonstrate that reproductive isolation arises from genomic rearrangements, whose frequency in starving yeast is several orders of magnitude greater than an unstarved control. By contrast, the frequency of point mutations is less than 2-fold greater. In a particular case, we observe that a starved lineage becomes reproductively isolated as a direct result of the stress-related accumulation of a single chromosome. We recapitulate this result by demonstrating that introducing an extra copy of one or several chromosomes into naïve, i.e. unstarved, yeast significantly diminishes their fertility. This type of reproductive barrier, whether arising spontaneously or via genetic manipulation, can be removed by making a lineage euploid for the altered chromosomes. Our model provides direct genetic evidence that reproductive isolation can arise frequently in stressed populations via genome restructuring without the precondition of geographic isolation. Public Library of Science 2013-07-24 /pmc/articles/PMC3722211/ /pubmed/23894280 http://dx.doi.org/10.1371/journal.pone.0066414 Text en © 2013 Kroll et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Kroll, Evgueny
Coyle, Scott
Dunn, Barbara
Koniges, Gregory
Aragon, Anthony
Edwards, Jeremy
Rosenzweig, Frank
Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title_full Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title_fullStr Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title_full_unstemmed Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title_short Starvation-Associated Genome Restructuring Can Lead to Reproductive Isolation in Yeast
title_sort starvation-associated genome restructuring can lead to reproductive isolation in yeast
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3722211/
https://www.ncbi.nlm.nih.gov/pubmed/23894280
http://dx.doi.org/10.1371/journal.pone.0066414
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