Cargando…

Collective motion conceals fitness differences in crowded cellular populations

Many cellular populations are tightly-packed, such as microbial colonies and biofilms, or tissues and tumors in multicellular organisms. Movement of one cell in those crowded assemblages requires motion of others, so that cell displacements are correlated over many cell diameters. Whenever movement...

Descripción completa

Detalles Bibliográficos
Autores principales: Kayser, Jona, Schreck, Carl F., Gralka, Matti, Fusco, Diana, Hallatschek, Oskar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6309230/
https://www.ncbi.nlm.nih.gov/pubmed/30510177
http://dx.doi.org/10.1038/s41559-018-0734-9
_version_ 1783383357639360512
author Kayser, Jona
Schreck, Carl F.
Gralka, Matti
Fusco, Diana
Hallatschek, Oskar
author_facet Kayser, Jona
Schreck, Carl F.
Gralka, Matti
Fusco, Diana
Hallatschek, Oskar
author_sort Kayser, Jona
collection PubMed
description Many cellular populations are tightly-packed, such as microbial colonies and biofilms, or tissues and tumors in multicellular organisms. Movement of one cell in those 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. Yet, 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 neighboring 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 neighbors through inevitable mechanical interactions. This effect has to be considered when predicting evolutionary outcomes, such as the emergence of drug resistance or cancer evolution.
format Online
Article
Text
id pubmed-6309230
institution National Center for Biotechnology Information
language English
publishDate 2018
record_format MEDLINE/PubMed
spelling pubmed-63092302019-06-03 Collective motion conceals fitness differences in crowded cellular populations Kayser, Jona Schreck, Carl F. Gralka, Matti Fusco, Diana Hallatschek, Oskar Nat Ecol Evol Article Many cellular populations are tightly-packed, such as microbial colonies and biofilms, or tissues and tumors in multicellular organisms. Movement of one cell in those 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. Yet, 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 neighboring 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 neighbors through inevitable mechanical interactions. This effect has to be considered when predicting evolutionary outcomes, such as the emergence of drug resistance or cancer evolution. 2018-12-03 2019-01 /pmc/articles/PMC6309230/ /pubmed/30510177 http://dx.doi.org/10.1038/s41559-018-0734-9 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Kayser, Jona
Schreck, Carl F.
Gralka, Matti
Fusco, Diana
Hallatschek, Oskar
Collective motion conceals fitness differences in crowded cellular populations
title Collective motion conceals fitness differences in crowded cellular populations
title_full Collective motion conceals fitness differences in crowded cellular populations
title_fullStr Collective motion conceals fitness differences in crowded cellular populations
title_full_unstemmed Collective motion conceals fitness differences in crowded cellular populations
title_short Collective motion conceals fitness differences in crowded cellular populations
title_sort collective motion conceals fitness differences in crowded cellular populations
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6309230/
https://www.ncbi.nlm.nih.gov/pubmed/30510177
http://dx.doi.org/10.1038/s41559-018-0734-9
work_keys_str_mv AT kayserjona collectivemotionconcealsfitnessdifferencesincrowdedcellularpopulations
AT schreckcarlf collectivemotionconcealsfitnessdifferencesincrowdedcellularpopulations
AT gralkamatti collectivemotionconcealsfitnessdifferencesincrowdedcellularpopulations
AT fuscodiana collectivemotionconcealsfitnessdifferencesincrowdedcellularpopulations
AT hallatschekoskar collectivemotionconcealsfitnessdifferencesincrowdedcellularpopulations