What Do We Mean by Multicellularity? The Evolutionary Transitions Framework Provides Answers

Rose, Caroline J.; Hammerschmidt, Katrin

doi:10.3389/fevo.2021.730714

Cited by 21 publications

(21 citation statements)

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“…Thus, at least some (if not all) transitions to differentiated multicellularity might have been a rewiring from temporal differentiation of life cycle stages to spatial differentiation in multicellular organisms (35). This poses important questions regarding the ease of such transitions, the ease of reversals to unicellularity, but also regarding our views of the transition to multicellularity (36). Should we really think about the transition to clonal multicellularity as the multi-step process that starts with the evolution of undifferentiated multicellularity getting more complex over evolutionary timescales or rather as a one-step process starting with a complex unicellular ancestor that directly transitions into a differentiated multicellular organism?…”

Section: Discussionmentioning

confidence: 99%

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

S¹,

Pichugin

Hammerschmidt³

2021

Preprint

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Understanding the evolutionary transition to multicellularity is a key problem in evolutionary biology (1,2). While around 25 independent instances of the evolution of multicellular existence are known across the tree of life (3), the ecological conditions that drive such transformations are not well understood. The first known transition to multicellularity occurred approximately 2.5 billion years ago in cyanobacteria (4,5,6), and today's cyanobacteria are characterized by an enormous morphological diversity, ranging from single-celled species over simple filamentous to highly differentiated filamentous ones (7,8). While the cyanobacterium Cyanothece sp. ATCC 51142 was isolated from the intertidal zone of the U.S. Gulf Coast as a unicellular species (9), we are first to additionally report a phenotypically mixed strategy where multicellular filaments and unicellular stages alternate. We experimentally demonstrate that the facultative multicellular life cycle depends on environmental conditions, such as salinity and population density, and use a theoretical model to explore the process of filament dissolution. While results predict that the observed response can be caused by an excreted compound in the medium, we cannot fully exclude changes in nutrient availability (as in (10,11)). The best fit modeling results demonstrate a nonlinear effect of the compound, which is characteristic for density-dependent sensing systems (12,13). Further, filament fragmentation is predicted to occur by means of connection cleavage rather than by cell death of every alternate cell. The phenotypic switch between the single-celled and multicellular morphology constitutes an environmentally dependent life cycle, which likely represents an important step en route to permanent multicellularity.

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Section: Discussionmentioning

confidence: 99%

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

S¹,

Pichugin

Hammerschmidt³

2021

Preprint

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“…Multicellularity has been defined in a variety of ways, ranging from functionally independent cells clumping as groups to indivisible multicellular entities (Hammerschmidt and Rose, 2021). Such associations can be "egalitarian" where cells do not derive from a recent common ancestor (Queller, 1997).…”

Section: The Evolution Of Multicellularity Egalitarian and Fraternal Associationsmentioning

confidence: 99%

“…Mathematical models suggest that a wide variety of factors favors such transitions from a solitary cell to a grouped state (Staps et al, 2021). This would be Stage 1 in the evolution of multicellularity, where each cell directly benefits from being in a larger association (Hammerschmidt and Rose, 2021). The evolutionary transition to Stage 2 occurs when group-level reproductive success becomes dependent on cooperation between cells, and entire assemblages act as multicellular individuals (Hammerschmidt and Rose, 2021).…”

Section: Simple Multicellularitymentioning

confidence: 99%

“…Simple multicellularity is also not considered a MET (Table 1) because it is neither a fully formed, higher-level individual nor a novel form of information storage or transmission. Simple multicellularity would appear in Figure 1 only as a 'new biological innovation' that was needed for the eventual MET of complex multicellularity (Stage 3: with obligate ontogeny of differentiated tissues; Hammerschmidt and Rose, 2021).…”

Section: Simple Multicellularitymentioning

confidence: 99%

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Major Evolutionary Transitions and the Roles of Facilitation and Information in Ecosystem Transformations

et al. 2021

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A small number of extraordinary “Major Evolutionary Transitions” (METs) have attracted attention among biologists. They comprise novel forms of individuality and information, and are defined in relation to organismal complexity, irrespective of broader ecosystem-level effects. This divorce between evolutionary and ecological consequences qualifies unicellular eukaryotes, for example, as a MET although they alone failed to significantly alter ecosystems. Additionally, this definition excludes revolutionary innovations not fitting into either MET type (e.g., photosynthesis). We recombine evolution with ecology to explore how and why entire ecosystems were newly created or radically altered – as Major System Transitions (MSTs). In doing so, we highlight important morphological adaptations that spread through populations because of their immediate, direct-fitness advantages for individuals. These are Major Competitive Transitions, or MCTs. We argue that often multiple METs and MCTs must be present to produce MSTs. For example, sexually-reproducing, multicellular eukaryotes (METs) with anisogamy and exoskeletons (MCTs) significantly altered ecosystems during the Cambrian. Therefore, we introduce the concepts of Facilitating Evolutionary Transitions (FETs) and Catalysts as key events or agents that are insufficient themselves to set a MST into motion, but are essential parts of synergies that do. We further elucidate the role of information in MSTs as transitions across five levels: (I) Encoded; (II) Epigenomic; (III) Learned; (IV) Inscribed; and (V) Dark Information. The latter is ‘authored’ by abiotic entities rather than biological organisms. Level IV has arguably allowed humans to produce a MST, and V perhaps makes us a FET for a future transition that melds biotic and abiotic life into one entity. Understanding the interactive processes involved in past major transitions will illuminate both current events and the surprising possibilities that abiotically-created information may produce.

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“…Defining when a lineage makes the transition to multicellularity can be challenging: some authors use the term ‘multicellular’ to simply mean that multiple cells are physically attached [7, 8], while others require that groups possess specific traits (e.g., cellular differentiation [9], etc.). In this paper, we use Peter Godfrey Smith’s Darwinian Individuality framework [10]: a group of cells makes the transition to multicellularity and becomes a Darwinian individual when it participates in the process of Darwinian evolution, gaining multicellular adaptations [11].…”

Section: Introductionmentioning

confidence: 99%

Evolutionary consequences of nascent multicellular life cycles

Pentz

MacGillivray

DuBose

et al. 2022

Preprint

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During the evolution of multicellularity, cells undergo an evolutionary transition in individuality, such that groups become the subject of Darwinian evolution. Comparative work, supported by theory, suggests that a life cycle in which cells 'stay together' following cellular division (termed clonal development) should facilitate this transition. While central to our understanding of multicellular evolution, this hypothesis has never been directly tested in a single experimental system. We circumvent this limitation by creating an isogenic yeast system capable of either clonal or aggregative development. We evolved 20 populations of either clonally-reproducing 'snowflake' yeast or aggregative 'floc' yeast with daily selection for rapid growth followed by sedimentation, an environment where multicellularity is adaptive. While both genotypes adapted to this regime, growing faster and having higher survival during the group-selection phase, there was a stark difference in evolutionary dynamics. Competitions reveal that evolved floc obtained nearly all of their increased fitness from faster growth, not improved group survival, while snowflake yeast mainly benefited from higher group-dependent fitness. Through a combination of genome sequencing and mathematical modeling, we identify a trade-off: clonal development can allow selection to act more efficiently on group-beneficial traits, but dramatically increases the overall rate of genetic drift due to mutational bottlenecking. Our results demonstrate how simple differences in the mode of group formation can have profound impacts on the transition to multicellularity: clonal development, but not aggregation, precipitated a transition from cells to groups as the primary level of Darwinian individuality.

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What Do We Mean by Multicellularity? The Evolutionary Transitions Framework Provides Answers

Cited by 21 publications

References 50 publications

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

Phenotypic plasticity, life cycles, and the evolutionary transition to multicellularity

Major Evolutionary Transitions and the Roles of Facilitation and Information in Ecosystem Transformations

Evolutionary consequences of nascent multicellular life cycles

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