The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity

Early multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells...

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Main Authors: Hanna Isaksson, Peter L. Conlin, Ben Kerr, William C. Ratcliff, Eric Libby
Format: Article
Language:English
Published: MDPI AG 2021-04-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/5/661
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author Hanna Isaksson
Peter L. Conlin
Ben Kerr
William C. Ratcliff
Eric Libby
author_facet Hanna Isaksson
Peter L. Conlin
Ben Kerr
William C. Ratcliff
Eric Libby
author_sort Hanna Isaksson
collection DOAJ
description Early multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells, whether they reproduce via binary fission or budding, can affect the rate of adaptation in primitive multicellularity. We use mathematical models to study the spread of beneficial, growth rate mutations in unicellular populations and populations of multicellular filaments reproducing via binary fission or budding. Comparing populations once they reach carrying capacity, we find that the spread of mutations in multicellular budding populations is qualitatively distinct from the other populations and in general slower. Since budding and binary fission distribute age-accumulated damage differently, we consider the effects of cellular senescence. When growth rate decreases with cell age, we find that beneficial mutations can spread significantly faster in a multicellular budding population than its corresponding unicellular population or a population reproducing via binary fission. Our results demonstrate that basic aspects of the cell cycle can give rise to different rates of adaptation in multicellular organisms.
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spelling doaj.art-d7fe3ee548334f099d52386826821a3e2023-11-21T17:34:52ZengMDPI AGGenes2073-44252021-04-0112566110.3390/genes12050661The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive MulticellularityHanna Isaksson0Peter L. Conlin1Ben Kerr2William C. Ratcliff3Eric Libby4Department of Mathematics and Mathematical Statistics, Umeå University, 90187 Umeå, SwedenGeorgia Institute of Technology, School of Biological Sciences, Atlanta, GA 30332, USADepartment of Biology, BEACON Center for the Study of Evolution in Action, University of Washington, Seattle, WA 98195, USAGeorgia Institute of Technology, School of Biological Sciences, Atlanta, GA 30332, USADepartment of Mathematics and Mathematical Statistics, Umeå University, 90187 Umeå, SwedenEarly multicellular organisms must gain adaptations to outcompete their unicellular ancestors, as well as other multicellular lineages. The tempo and mode of multicellular adaptation is influenced by many factors including the traits of individual cells. We consider how a fundamental aspect of cells, whether they reproduce via binary fission or budding, can affect the rate of adaptation in primitive multicellularity. We use mathematical models to study the spread of beneficial, growth rate mutations in unicellular populations and populations of multicellular filaments reproducing via binary fission or budding. Comparing populations once they reach carrying capacity, we find that the spread of mutations in multicellular budding populations is qualitatively distinct from the other populations and in general slower. Since budding and binary fission distribute age-accumulated damage differently, we consider the effects of cellular senescence. When growth rate decreases with cell age, we find that beneficial mutations can spread significantly faster in a multicellular budding population than its corresponding unicellular population or a population reproducing via binary fission. Our results demonstrate that basic aspects of the cell cycle can give rise to different rates of adaptation in multicellular organisms.https://www.mdpi.com/2073-4425/12/5/661binary fissionbuddingmulticellularityagingadaptationfilaments
spellingShingle Hanna Isaksson
Peter L. Conlin
Ben Kerr
William C. Ratcliff
Eric Libby
The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
Genes
binary fission
budding
multicellularity
aging
adaptation
filaments
title The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
title_full The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
title_fullStr The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
title_full_unstemmed The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
title_short The Consequences of Budding versus Binary Fission on Adaptation and Aging in Primitive Multicellularity
title_sort consequences of budding versus binary fission on adaptation and aging in primitive multicellularity
topic binary fission
budding
multicellularity
aging
adaptation
filaments
url https://www.mdpi.com/2073-4425/12/5/661
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