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Title: Collective motion conceals fitness differences in crowded cellular populations

Abstract

Many cellular populations are tightly packed, such as microbial colonies and biofilms, or tissues and tumours in multicellular organisms. The movement of one cell in these crowded assemblages requires motion of others, so that cell displacements are correlated over many cell diameters. Whenever movement is important for survival or growth, these correlated rearrangements could couple the evolutionary fate of different lineages. However, little is known about the interplay between mechanical forces and evolution in dense cellular populations. Here, by tracking slower-growing clones at the expanding edge of yeast colonies, we show that the collective motion of cells prevents costly mutations from being weeded out rapidly. Joint pushing by neighbouring cells generates correlated movements that suppress the differential displacements required for selection to act. This mechanical screening of fitness differences allows slower-growing mutants to leave more descendants than expected under non-mechanical models, thereby increasing their chance for evolutionary rescue. Our work suggests that, in crowded populations, cells cooperate with surrounding neighbours through inevitable mechanical interactions. This effect has to be considered when predicting evolutionary outcomes, such as the emergence of drug resistance or cancer evolution.

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Physics, and Dept. of Integrative Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1506392
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Nature Ecology and Evolution
Additional Journal Information:
Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 2397-334X
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Kayser, Jona, Schreck, Carl F., Gralka, Matti, Fusco, Diana, and Hallatschek, Oskar. Collective motion conceals fitness differences in crowded cellular populations. United States: N. p., 2018. Web. doi:10.1038/s41559-018-0734-9.
Kayser, Jona, Schreck, Carl F., Gralka, Matti, Fusco, Diana, & Hallatschek, Oskar. Collective motion conceals fitness differences in crowded cellular populations. United States. doi:10.1038/s41559-018-0734-9.
Kayser, Jona, Schreck, Carl F., Gralka, Matti, Fusco, Diana, and Hallatschek, Oskar. Mon . "Collective motion conceals fitness differences in crowded cellular populations". United States. doi:10.1038/s41559-018-0734-9. https://www.osti.gov/servlets/purl/1506392.
@article{osti_1506392,
title = {Collective motion conceals fitness differences in crowded cellular populations},
author = {Kayser, Jona and Schreck, Carl F. and Gralka, Matti and Fusco, Diana and Hallatschek, Oskar},
abstractNote = {Many cellular populations are tightly packed, such as microbial colonies and biofilms, or tissues and tumours in multicellular organisms. The movement of one cell in these crowded assemblages requires motion of others, so that cell displacements are correlated over many cell diameters. Whenever movement is important for survival or growth, these correlated rearrangements could couple the evolutionary fate of different lineages. However, little is known about the interplay between mechanical forces and evolution in dense cellular populations. Here, by tracking slower-growing clones at the expanding edge of yeast colonies, we show that the collective motion of cells prevents costly mutations from being weeded out rapidly. Joint pushing by neighbouring cells generates correlated movements that suppress the differential displacements required for selection to act. This mechanical screening of fitness differences allows slower-growing mutants to leave more descendants than expected under non-mechanical models, thereby increasing their chance for evolutionary rescue. Our work suggests that, in crowded populations, cells cooperate with surrounding neighbours through inevitable mechanical interactions. This effect has to be considered when predicting evolutionary outcomes, such as the emergence of drug resistance or cancer evolution.},
doi = {10.1038/s41559-018-0734-9},
journal = {Nature Ecology and Evolution},
issn = {2397-334X},
number = 1,
volume = 3,
place = {United States},
year = {2018},
month = {12}
}

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