A unified framework for measuring selection on cellular lineages and traits
Intracellular states probed by gene expression profiles and metabolic activities are intrinsically noisy, causing phenotypic variations among cellular lineages. Understanding the adaptive and evolutionary roles of such variations requires clarifying their linkage to population growth rates. Extendin...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-12-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/72299 |
| _version_ | 1811212540061941760 |
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| author | Shunpei Yamauchi Takashi Nozoe Reiko Okura Edo Kussell Yuichi Wakamoto |
| author_facet | Shunpei Yamauchi Takashi Nozoe Reiko Okura Edo Kussell Yuichi Wakamoto |
| author_sort | Shunpei Yamauchi |
| collection | DOAJ |
| description | Intracellular states probed by gene expression profiles and metabolic activities are intrinsically noisy, causing phenotypic variations among cellular lineages. Understanding the adaptive and evolutionary roles of such variations requires clarifying their linkage to population growth rates. Extending a cell lineage statistics framework, here we show that a population’s growth rate can be expanded by the cumulants of a fitness landscape that characterize how fitness distributes in a population. The expansion enables quantifying the contribution of each cumulant, such as variance and skewness, to population growth. We introduce a function that contains all the essential information of cell lineage statistics, including mean lineage fitness and selection strength. We reveal a relation between fitness heterogeneity and population growth rate response to perturbation. We apply the framework to experimental cell lineage data from bacteria to mammalian cells, revealing distinct levels of growth rate gain from fitness heterogeneity across environments and organisms. Furthermore, third or higher order cumulants’ contributions are negligible under constant growth conditions but could be significant in regrowing processes from growth-arrested conditions. We identify cellular populations in which selection leads to an increase of fitness variance among lineages in retrospective statistics compared to chronological statistics. The framework assumes no particular growth models or environmental conditions, and is thus applicable to various biological phenomena for which phenotypic heterogeneity and cellular proliferation are important. |
| first_indexed | 2024-04-12T05:30:40Z |
| format | Article |
| id | doaj.art-ed0070732bcf430599c3e50827de9672 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T05:30:40Z |
| publishDate | 2022-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-ed0070732bcf430599c3e50827de96722022-12-22T03:46:06ZengeLife Sciences Publications LtdeLife2050-084X2022-12-011110.7554/eLife.72299A unified framework for measuring selection on cellular lineages and traitsShunpei Yamauchi0https://orcid.org/0000-0002-8530-4147Takashi Nozoe1https://orcid.org/0000-0003-2556-6484Reiko Okura2Edo Kussell3https://orcid.org/0000-0003-0590-4036Yuichi Wakamoto4https://orcid.org/0000-0002-6233-0844Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, JapanDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, JapanDepartment of Biology, New York University, New York, United States; Department of Physics, New York University, New York, United StatesDepartment of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan; Research Center for Complex Systems Biology, The University of Tokyo, Tokyo, Japan; Universal Biology Institute, The University of Tokyo, Tokyo, JapanIntracellular states probed by gene expression profiles and metabolic activities are intrinsically noisy, causing phenotypic variations among cellular lineages. Understanding the adaptive and evolutionary roles of such variations requires clarifying their linkage to population growth rates. Extending a cell lineage statistics framework, here we show that a population’s growth rate can be expanded by the cumulants of a fitness landscape that characterize how fitness distributes in a population. The expansion enables quantifying the contribution of each cumulant, such as variance and skewness, to population growth. We introduce a function that contains all the essential information of cell lineage statistics, including mean lineage fitness and selection strength. We reveal a relation between fitness heterogeneity and population growth rate response to perturbation. We apply the framework to experimental cell lineage data from bacteria to mammalian cells, revealing distinct levels of growth rate gain from fitness heterogeneity across environments and organisms. Furthermore, third or higher order cumulants’ contributions are negligible under constant growth conditions but could be significant in regrowing processes from growth-arrested conditions. We identify cellular populations in which selection leads to an increase of fitness variance among lineages in retrospective statistics compared to chronological statistics. The framework assumes no particular growth models or environmental conditions, and is thus applicable to various biological phenomena for which phenotypic heterogeneity and cellular proliferation are important.https://elifesciences.org/articles/72299cell lineage statisticsphenotypic heterogeneityselection strengthfitnesscumulantpopulation growth rate |
| spellingShingle | Shunpei Yamauchi Takashi Nozoe Reiko Okura Edo Kussell Yuichi Wakamoto A unified framework for measuring selection on cellular lineages and traits eLife cell lineage statistics phenotypic heterogeneity selection strength fitness cumulant population growth rate |
| title | A unified framework for measuring selection on cellular lineages and traits |
| title_full | A unified framework for measuring selection on cellular lineages and traits |
| title_fullStr | A unified framework for measuring selection on cellular lineages and traits |
| title_full_unstemmed | A unified framework for measuring selection on cellular lineages and traits |
| title_short | A unified framework for measuring selection on cellular lineages and traits |
| title_sort | unified framework for measuring selection on cellular lineages and traits |
| topic | cell lineage statistics phenotypic heterogeneity selection strength fitness cumulant population growth rate |
| url | https://elifesciences.org/articles/72299 |
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