Evolution of simple multicellular life cycles in dynamic environments

Pichugin, Yuriy; Park, Hye Jin; Traulsen, Arne

doi:10.1098/rsif.2019.0054

Cited by 25 publications

(25 citation statements)

References 58 publications

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“…that by producing small propagules, single-species groups are able to persist in the presence of high mutation rates. Recently Pichugin, Peña, Rainey, Traulsen [ 5 ], Pichugin, Traulsen [ 28 ], and Pichugin, Park, Traulsen [ 29 ] developed an analytical framework which they used to calculate the optimal fragmentation mode for simple single-species groups in the absence of mutations. Their modelling approach is very different form ours, but is used to address similar questions.…”

Section: Discussionmentioning

confidence: 99%

“…While this research program has been fruitful and insightful, it considers only a limited set of propagule production strategies (viz., the production of a propagule of varying size). Recent research by Pichugin, Traulsen, and collaborators [ 5 , 28 , 29 ] has started to address the wide variety of strategies that exist in nature. Their models exhaustively analyse the fitness consequences of every mathematically possible partition of multicellular groups.…”

Section: Introductionmentioning

confidence: 99%

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Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

2021

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Reproduction is one of the requirements for evolution and a defining feature of life. Yet, across the tree of life, organisms reproduce in many different ways. Groups of cells (e.g., multicellular organisms, colonial microbes, or multispecies biofilms) divide by releasing propagules that can be single-celled or multicellular. What conditions determine the number and size of reproductive propagules? In multicellular organisms, existing theory suggests that single-cell propagules prevent the accumulation of deleterious mutations (e.g., cheaters). However, groups of cells, such as biofilms, sometimes contain multiple metabolically interdependent species. This creates a reproductive dilemma: small daughter groups, which prevent the accumulation of cheaters, are also unlikely to contain the species diversity that is required for ecological success. Here, we developed an individual-based, multilevel selection model to investigate how such multi-species groups can resolve this dilemma. By tracking the dynamics of groups of cells that reproduce by fragmenting into smaller groups, we identified fragmentation modes that can maintain cooperative interactions. We systematically varied the fragmentation mode and calculated the maximum mutation rate that communities can withstand before being driven to extinction by the accumulation of cheaters. We find that for groups consisting of a single species, the optimal fragmentation mode consists of releasing single-cell propagules. For multi-species groups we find various optimal strategies. With migration between groups, single-cell propagules are favored. Without migration, larger propagules sizes are optimal; in this case, group-size dependent fissioning rates can prevent the accumulation of cheaters. Our work shows that multi-species groups can evolve reproductive strategies that allow them to maintain cooperative interactions.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

2021

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“…Moreover, even stages of highly sophisticated and integrated developmental animal life cycles have been discovered to depend on external factors and ecological triggers, some of which are based on communication with external bacteria (25). Theoretical models of life cycle evolution have shown that a changing environment can lead to the evolution of complex life cycles in which some cells live and reproduce as unicellular beings, while others form groups (26).…”

Section: Phenotypic Plasticity and Evolutionary Transitions In Multicellularitymentioning

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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“…The particular mode by which the earliest multicellular groups reproduce, for example through a dedicated (germ) cell or by fragmentation, has implications for their ability to transition in individuality and participate in natural selection (Ratcliff et al, 2012;Hammerschmidt et al, 2014). Furthermore, during this transitional phase, ecological conditions are of critical importance (Pichugin et al, 2019;Staps et al, 2019), such as structured environments that maintain the discreteness of groups, and crucially, their reproductive cells (Rose et al, 2020). Such conditions provide the ecological scaffold for selection to act on less-integrated groups until they complete the transition to 'multicellular individuals' (Black et al, 2020).…”

Section: Stage Two -Evolution Of Multicellular Individualsmentioning

confidence: 99%

What do we mean by multicellularity? The Evolutionary Transitions Framework provides answers

Rose¹,

Hammerschmidt²

2021

Preprint

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The meaning of the word ‘multicellularity’ appears to be unambiguous – a concept that can be grasped with common sense. On closer inspection, however, there is notable disparity in the recent literature regarding the usage of the term ‘multicellularity’, which can describe complex organisms, simple microbial colonies or even multi-species biofilms. In addition, while emerging research directions, such as ‘the evolutionary transition to multicellularity’, have brought together a highly interdisciplinary community of researchers, they tend to (mis)use historically relevant language that does not adequately describe the marginal or nascent cases of multicellularity that are the focus of this new field. We argue that clarity can be achieved with the realisation that the various definitions of multicellularity are in fact describing different stages that can occur during the course of evolution. With the aim of gaining semantic continuity among researchers in this broad field, we provide a framework for identifying the stages of the evolutionary transition to multicellularity: from multicellular groups, to multicellular individuals, and finally to multicellular organisms.

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Evolution of simple multicellular life cycles in dynamic environments

Cited by 25 publications

References 58 publications

Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities

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

What do we mean by multicellularity? The Evolutionary Transitions Framework provides answers

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