Heterogeneous individual motility biases group composition in a model of aggregating cells

Detalhes bibliográficos
Autor(a) principal: Forget, Mathieu
Data de Publicação: 2022
Outros Autores: Adiba, Sandrine, Brunnet, Leonardo Gregory, De Monte, Silvia
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFRGS
Texto Completo: http://hdl.handle.net/10183/254242
Resumo: Aggregative life cycles are characterized by alternating phases of unicellular growth and multicellular development. Their multiple, independent evolutionary emergence suggests that they may have coopted pervasive properties of single-celled ancestors. Primitive multicellular aggregates, where coordination mechanisms were less efficient than in extant aggregative microbes, must have faced high levels of conflict between different co-aggregating populations. Such conflicts within a multicellular body manifest in the differential reproductive output of cells of different types. Here, we study how heterogeneity in cell motility affects the aggregation process and creates a mismatch between the composition of the population and that of self-organized groups of active adhesive particles. We model cells as self-propelled particles and describe aggregation in a plane starting from a dispersed configuration. Inspired by the life cycle of aggregative model organisms such as Dictyostelium discoideum or Myxococcus xanthus, whose cells interact for a fixed duration before the onset of chimeric multicellular development, we study finite-time configurations for identical particles and in binary mixes. We show that co-aggregation results in three different types of frequency-dependent biases, one of which is associated to evolutionarily stable coexistence of particles with different motility. We propose a heuristic explanation of such observations, based on the competition between delayed aggregation of slower particles and detachment of faster particles. Unexpectedly, despite the complexity and non-linearity of the system, biases can be largely predicted from the behavior of the two corresponding homogenous populations. This model points to differential motility as a possibly important factor in driving the evolutionary emergence of facultatively multicellular life-cycles.
id UFRGS-2_ed6dc5c1fa29a9cc172babaa7dc8cbc8
oai_identifier_str oai:www.lume.ufrgs.br:10183/254242
network_acronym_str UFRGS-2
network_name_str Repositório Institucional da UFRGS
repository_id_str
spelling Forget, MathieuAdiba, SandrineBrunnet, Leonardo GregoryDe Monte, Silvia2023-02-07T05:02:10Z20222296-701Xhttp://hdl.handle.net/10183/254242001160356Aggregative life cycles are characterized by alternating phases of unicellular growth and multicellular development. Their multiple, independent evolutionary emergence suggests that they may have coopted pervasive properties of single-celled ancestors. Primitive multicellular aggregates, where coordination mechanisms were less efficient than in extant aggregative microbes, must have faced high levels of conflict between different co-aggregating populations. Such conflicts within a multicellular body manifest in the differential reproductive output of cells of different types. Here, we study how heterogeneity in cell motility affects the aggregation process and creates a mismatch between the composition of the population and that of self-organized groups of active adhesive particles. We model cells as self-propelled particles and describe aggregation in a plane starting from a dispersed configuration. Inspired by the life cycle of aggregative model organisms such as Dictyostelium discoideum or Myxococcus xanthus, whose cells interact for a fixed duration before the onset of chimeric multicellular development, we study finite-time configurations for identical particles and in binary mixes. We show that co-aggregation results in three different types of frequency-dependent biases, one of which is associated to evolutionarily stable coexistence of particles with different motility. We propose a heuristic explanation of such observations, based on the competition between delayed aggregation of slower particles and detachment of faster particles. Unexpectedly, despite the complexity and non-linearity of the system, biases can be largely predicted from the behavior of the two corresponding homogenous populations. This model points to differential motility as a possibly important factor in driving the evolutionary emergence of facultatively multicellular life-cycles.application/pdfengFrontiers in Ecology and Evolution. Lausanne. Vol. 10 (Dec. 2022), 1052309, 18 p.Biologia evolutivaAgregacaoSimulação computacionalDinâmica populacionalMulticellularityEvolutionSelf-propelled particle systemsAggregationMotilityHeterogeneityHeterogeneous individual motility biases group composition in a model of aggregating cellsEstrangeiroinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFRGSinstname:Universidade Federal do Rio Grande do Sul (UFRGS)instacron:UFRGSTEXT001160356.pdf.txt001160356.pdf.txtExtracted Texttext/plain85006http://www.lume.ufrgs.br/bitstream/10183/254242/2/001160356.pdf.txt965fa1f89119bd78cad5cd1c2776a1afMD52ORIGINAL001160356.pdfTexto completo (inglês)application/pdf2542686http://www.lume.ufrgs.br/bitstream/10183/254242/1/001160356.pdfaa81b9e6d7731e7b4bb3f46987c58803MD5110183/2542422024-05-18 06:24:24.717793oai:www.lume.ufrgs.br:10183/254242Repositório de PublicaçõesPUBhttps://lume.ufrgs.br/oai/requestopendoar:2024-05-18T09:24:24Repositório Institucional da UFRGS - Universidade Federal do Rio Grande do Sul (UFRGS)false
dc.title.pt_BR.fl_str_mv Heterogeneous individual motility biases group composition in a model of aggregating cells
title Heterogeneous individual motility biases group composition in a model of aggregating cells
spellingShingle Heterogeneous individual motility biases group composition in a model of aggregating cells
Forget, Mathieu
Biologia evolutiva
Agregacao
Simulação computacional
Dinâmica populacional
Multicellularity
Evolution
Self-propelled particle systems
Aggregation
Motility
Heterogeneity
title_short Heterogeneous individual motility biases group composition in a model of aggregating cells
title_full Heterogeneous individual motility biases group composition in a model of aggregating cells
title_fullStr Heterogeneous individual motility biases group composition in a model of aggregating cells
title_full_unstemmed Heterogeneous individual motility biases group composition in a model of aggregating cells
title_sort Heterogeneous individual motility biases group composition in a model of aggregating cells
author Forget, Mathieu
author_facet Forget, Mathieu
Adiba, Sandrine
Brunnet, Leonardo Gregory
De Monte, Silvia
author_role author
author2 Adiba, Sandrine
Brunnet, Leonardo Gregory
De Monte, Silvia
author2_role author
author
author
dc.contributor.author.fl_str_mv Forget, Mathieu
Adiba, Sandrine
Brunnet, Leonardo Gregory
De Monte, Silvia
dc.subject.por.fl_str_mv Biologia evolutiva
Agregacao
Simulação computacional
Dinâmica populacional
topic Biologia evolutiva
Agregacao
Simulação computacional
Dinâmica populacional
Multicellularity
Evolution
Self-propelled particle systems
Aggregation
Motility
Heterogeneity
dc.subject.eng.fl_str_mv Multicellularity
Evolution
Self-propelled particle systems
Aggregation
Motility
Heterogeneity
description Aggregative life cycles are characterized by alternating phases of unicellular growth and multicellular development. Their multiple, independent evolutionary emergence suggests that they may have coopted pervasive properties of single-celled ancestors. Primitive multicellular aggregates, where coordination mechanisms were less efficient than in extant aggregative microbes, must have faced high levels of conflict between different co-aggregating populations. Such conflicts within a multicellular body manifest in the differential reproductive output of cells of different types. Here, we study how heterogeneity in cell motility affects the aggregation process and creates a mismatch between the composition of the population and that of self-organized groups of active adhesive particles. We model cells as self-propelled particles and describe aggregation in a plane starting from a dispersed configuration. Inspired by the life cycle of aggregative model organisms such as Dictyostelium discoideum or Myxococcus xanthus, whose cells interact for a fixed duration before the onset of chimeric multicellular development, we study finite-time configurations for identical particles and in binary mixes. We show that co-aggregation results in three different types of frequency-dependent biases, one of which is associated to evolutionarily stable coexistence of particles with different motility. We propose a heuristic explanation of such observations, based on the competition between delayed aggregation of slower particles and detachment of faster particles. Unexpectedly, despite the complexity and non-linearity of the system, biases can be largely predicted from the behavior of the two corresponding homogenous populations. This model points to differential motility as a possibly important factor in driving the evolutionary emergence of facultatively multicellular life-cycles.
publishDate 2022
dc.date.issued.fl_str_mv 2022
dc.date.accessioned.fl_str_mv 2023-02-07T05:02:10Z
dc.type.driver.fl_str_mv Estrangeiro
info:eu-repo/semantics/article
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10183/254242
dc.identifier.issn.pt_BR.fl_str_mv 2296-701X
dc.identifier.nrb.pt_BR.fl_str_mv 001160356
identifier_str_mv 2296-701X
001160356
url http://hdl.handle.net/10183/254242
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Frontiers in Ecology and Evolution. Lausanne. Vol. 10 (Dec. 2022), 1052309, 18 p.
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Repositório Institucional da UFRGS
instname:Universidade Federal do Rio Grande do Sul (UFRGS)
instacron:UFRGS
instname_str Universidade Federal do Rio Grande do Sul (UFRGS)
instacron_str UFRGS
institution UFRGS
reponame_str Repositório Institucional da UFRGS
collection Repositório Institucional da UFRGS
bitstream.url.fl_str_mv http://www.lume.ufrgs.br/bitstream/10183/254242/2/001160356.pdf.txt
http://www.lume.ufrgs.br/bitstream/10183/254242/1/001160356.pdf
bitstream.checksum.fl_str_mv 965fa1f89119bd78cad5cd1c2776a1af
aa81b9e6d7731e7b4bb3f46987c58803
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
repository.name.fl_str_mv Repositório Institucional da UFRGS - Universidade Federal do Rio Grande do Sul (UFRGS)
repository.mail.fl_str_mv
_version_ 1801225079728635904