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Single-cell adaptations shape evolutionary transitions to multicellularity in green algae

Cornwallis, Charlie K LU ; Svensson-Coelho, Maria LU ; Lindh, Markus LU ; Li, Qinyang LU orcid ; Stábile, Franca LU orcid ; Hansson, Lars-Anders LU orcid and Rengefors, Karin LU (2023) In Nature Ecology and Evolution 7(6). p.889-902
Abstract

The evolution of multicellular life has played a pivotal role in shaping biological diversity. However, we know surprisingly little about the natural environmental conditions that favour the formation of multicellular groups. Here we experimentally examine how key environmental factors (predation, nitrogen and water turbulence) combine to influence multicellular group formation in 35 wild unicellular green algae strains (19 Chlorophyta species). All environmental factors induced the formation of multicellular groups (more than four cells), but there was no evidence this was adaptive, as multicellularity (% cells in groups) was not related to population growth rate under any condition. Instead, population growth was related to... (More)

The evolution of multicellular life has played a pivotal role in shaping biological diversity. However, we know surprisingly little about the natural environmental conditions that favour the formation of multicellular groups. Here we experimentally examine how key environmental factors (predation, nitrogen and water turbulence) combine to influence multicellular group formation in 35 wild unicellular green algae strains (19 Chlorophyta species). All environmental factors induced the formation of multicellular groups (more than four cells), but there was no evidence this was adaptive, as multicellularity (% cells in groups) was not related to population growth rate under any condition. Instead, population growth was related to extracellular matrix (ECM) around single cells and palmelloid formation, a unicellular life-cycle stage where two to four cells are retained within a mother-cell wall after mitosis. ECM production increased with nitrogen levels resulting in more cells being in palmelloids and higher rates of multicellular group formation. Examining the distribution of 332 algae species across 478 lakes monitored over 55 years, showed that ECM and nitrogen availability also predicted patterns of obligate multicellularity in nature. Our results highlight that adaptations of unicellular organisms to cope with environmental challenges may be key to understanding evolutionary routes to multicellular life.

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author
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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Nature Ecology and Evolution
volume
7
issue
6
pages
889 - 902
publisher
Nature Publishing Group
external identifiers
  • pmid:37081145
  • scopus:85153380404
ISSN
2397-334X
DOI
10.1038/s41559-023-02044-6
language
English
LU publication?
yes
id
50de6f52-b2ca-4a50-874e-e1cd6a5ff516
date added to LUP
2023-05-10 12:04:08
date last changed
2024-06-15 02:49:05
@article{50de6f52-b2ca-4a50-874e-e1cd6a5ff516,
  abstract     = {{<p>The evolution of multicellular life has played a pivotal role in shaping biological diversity. However, we know surprisingly little about the natural environmental conditions that favour the formation of multicellular groups. Here we experimentally examine how key environmental factors (predation, nitrogen and water turbulence) combine to influence multicellular group formation in 35 wild unicellular green algae strains (19 Chlorophyta species). All environmental factors induced the formation of multicellular groups (more than four cells), but there was no evidence this was adaptive, as multicellularity (% cells in groups) was not related to population growth rate under any condition. Instead, population growth was related to extracellular matrix (ECM) around single cells and palmelloid formation, a unicellular life-cycle stage where two to four cells are retained within a mother-cell wall after mitosis. ECM production increased with nitrogen levels resulting in more cells being in palmelloids and higher rates of multicellular group formation. Examining the distribution of 332 algae species across 478 lakes monitored over 55 years, showed that ECM and nitrogen availability also predicted patterns of obligate multicellularity in nature. Our results highlight that adaptations of unicellular organisms to cope with environmental challenges may be key to understanding evolutionary routes to multicellular life.</p>}},
  author       = {{Cornwallis, Charlie K and Svensson-Coelho, Maria and Lindh, Markus and Li, Qinyang and Stábile, Franca and Hansson, Lars-Anders and Rengefors, Karin}},
  issn         = {{2397-334X}},
  language     = {{eng}},
  month        = {{04}},
  number       = {{6}},
  pages        = {{889--902}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Ecology and Evolution}},
  title        = {{Single-cell adaptations shape evolutionary transitions to multicellularity in green algae}},
  url          = {{http://dx.doi.org/10.1038/s41559-023-02044-6}},
  doi          = {{10.1038/s41559-023-02044-6}},
  volume       = {{7}},
  year         = {{2023}},
}