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Evolutionary consequences of nascent multicellular life cycles

A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in...

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Autores principales: Pentz, Jennifer T, MacGillivray, Kathryn, DuBose, James G, Conlin, Peter L, Reinhardt, Emma, Libby, Eric, Ratcliff, William C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611430/
https://www.ncbi.nlm.nih.gov/pubmed/37889142
http://dx.doi.org/10.7554/eLife.84336
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author Pentz, Jennifer T
MacGillivray, Kathryn
DuBose, James G
Conlin, Peter L
Reinhardt, Emma
Libby, Eric
Ratcliff, William C
author_facet Pentz, Jennifer T
MacGillivray, Kathryn
DuBose, James G
Conlin, Peter L
Reinhardt, Emma
Libby, Eric
Ratcliff, William C
author_sort Pentz, Jennifer T
collection PubMed
description A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing ‘snowflake’ yeast (Δace2/∆ace2) and aggregative ‘floc’ yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift—a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation.
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spelling pubmed-106114302023-10-28 Evolutionary consequences of nascent multicellular life cycles Pentz, Jennifer T MacGillivray, Kathryn DuBose, James G Conlin, Peter L Reinhardt, Emma Libby, Eric Ratcliff, William C eLife Evolutionary Biology A key step in the evolutionary transition to multicellularity is the origin of multicellular groups as biological individuals capable of adaptation. Comparative work, supported by theory, suggests clonal development should facilitate this transition, although this hypothesis has never been tested in a single model system. We evolved 20 replicate populations of otherwise isogenic clonally reproducing ‘snowflake’ yeast (Δace2/∆ace2) and aggregative ‘floc’ yeast (GAL1p::FLO1 /GAL1p::FLO1) with daily selection for rapid growth in liquid media, which favors faster cell division, followed by selection for rapid sedimentation, which favors larger multicellular groups. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Aggregative floc yeast obtained nearly all their increased fitness from faster growth, not improved group survival; indicating that selection acted primarily at the level of cells. In contrast, clonal snowflake yeast mainly benefited from higher group-dependent fitness, indicating a shift in the level of Darwinian individuality from cells to groups. Through genome sequencing and mathematical modeling, we show that the genetic bottlenecks in a clonal life cycle also drive much higher rates of genetic drift—a result with complex implications for this evolutionary transition. Our results highlight the central role that early multicellular life cycles play in the process of multicellular adaptation. eLife Sciences Publications, Ltd 2023-10-27 /pmc/articles/PMC10611430/ /pubmed/37889142 http://dx.doi.org/10.7554/eLife.84336 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Evolutionary Biology
Pentz, Jennifer T
MacGillivray, Kathryn
DuBose, James G
Conlin, Peter L
Reinhardt, Emma
Libby, Eric
Ratcliff, William C
Evolutionary consequences of nascent multicellular life cycles
title Evolutionary consequences of nascent multicellular life cycles
title_full Evolutionary consequences of nascent multicellular life cycles
title_fullStr Evolutionary consequences of nascent multicellular life cycles
title_full_unstemmed Evolutionary consequences of nascent multicellular life cycles
title_short Evolutionary consequences of nascent multicellular life cycles
title_sort evolutionary consequences of nascent multicellular life cycles
topic Evolutionary Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10611430/
https://www.ncbi.nlm.nih.gov/pubmed/37889142
http://dx.doi.org/10.7554/eLife.84336
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