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Title: Collective motion conceals fitness differences in crowded cellular populations

Journal Article · · Nature Ecology and Evolution

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1506392
Journal Information:
Nature Ecology and Evolution, Vol. 3, Issue 1; ISSN 2397-334X
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 16 works
Citation information provided by
Web of Science

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Cited By (3)

Environmental heterogeneity can tip the population genetics of range expansions journal April 2019
Nucleation of antagonistic organisms and cellular competitions on curved, inflating substrates journal October 2019
Physical interactions reduce the power of natural selection in growing yeast colonies journal October 2018

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